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FLEAS, FLUKES & CUCKOOS

THE NEW NATURALIST

EDITORS :

JAMES FISHER, M.A.

JOHN GILMOUR, M.A.

JULIAN HUXLEY, M.A., D.Sc, F.R.S.

L. DUDLEY STAMP, C.B.E., D.Litt., D.Sc.

PHOTOGRAPHIC EDITOR:

ERIC HOSKING, F.R.P.S.

THENEWNATURALIST ^ O^

FLEAS, FLUKES &
CUCKOOS

A STUDY OF BIRD PARASITES

MIRIAM ROTHSCHILD

and

THERESA CLAY

W\th gg Black and White Photographs
4 Maps & 22 Drawings

THE MACMILLAN COMPANY

NEW YORK

1957

Charles Rothschild

First published in igjs by

Collins 14 St. James's Place London

Printed in Great Britain

by Willmer Brothers & Co. Ltd.

Birkenhead

for Collins Clear- Type Press

London and Glasgow

CONTENTS

editors' preface
authors' preface

PART ONE
chapter

Introduction

1 Parasitism

2 Commensalism

3 Symbiosis

4 The Effect of Parasites on the Host

5 The Effect of Parasitism on the Parasite

page
ix

xii

1 1

30
38

6 The Origins of Parasitism and the Evolution of Parasites 47

Introduction

7 Fleas

8 Feather Lice

PART TWO

118

Introduction
9 Protozoa
10 Worms

PART THREE

158

159
176

CONTENTS

PAGE

11 Flies 2X1

12 Mites 224

13 Micro-Parasites 235

14 The Fauna of Birds' Nestb 245

15 Skuas 253

16 The European Cuckoo 256

BIBLIOGRAPHICAL APPENDIX 269

INDEX OF POPULAR AND SCIENTIFIC NAMES 283

GENERAL INDEX 296

INDEX OF SCIENTIFIC NAMES OF BIRDS MENTIONED

IN THE TEXT 302

ILLUSTRATIONS

FACING

PAGE

Starling Louse

Quill Louse

Great Spotted Woodpecker

III

Great Tit removing cap from milk bottle

IVa

Robin perched on spade

IVb

Hen Blackbird sunning

Phoresy

Barn-Owl feeding Rat to young

VII

Effect of parasite on host

/III

Young Starling preening

Louse-flies

Pronotal comb of Mammal Flea and Bird Flea

The two main types of Fleas

XII

Mouth-Parts showine: adaptations to specialised

methods of feeding 51

XIII-XIV The Receptaculum Seminis of Female British

Bird Fleas and Mammal Fleas 66-67

XV-XVI Terminal Portion of Male British Bird Fleas 82-83

XVII Common House-Martin Flea 98

XVIII Life-Cycle of Flea 99

XIX Pygidium of Flea 114

XX Swan 115

XXI
XXII
XXIII
XXIV
XXV
XXVI
XXVII
XXVI II
XXIX
XXX
XXXI
XXXII
XXXIIIa-b
XXXIIIc
XXXIVa
XXXIVb
XXXV
XXXVI
XXXVII
XXXVIIIa
XXXVIIIb
XXXIX
XL

ILLUSTRATIONS

Feather Louse from Common Tern 130

The two main types of Feather Lice 131

Different kinds of Feather Lice 146

Eggs of Wing Feather Louse 147

Trypanosoma 162

Sand-Martins preparing to migrate 163

Fluke, Roundworms and Tapeworm 178

Intermediate hosts of Herring-Gull Fluke 179

Biting Midge 210

Mosquitoes which feed on Birds 2 1 1

Feather Mites 226

Sheep Tick 227

Common House-Martin Flea 242

Leg of Shearwater Flea 242

Cormorant Colony 243

Shearwater at entrance to its burrow 243

Sand-Martin at nest burrow 258

Bed-bug and Swallow-bug 259

White throat removing parasites ? 264

Arctic Skua * 265

The Cuckoo 265
House-Martins collecting mud for their nests 268

Birds congregating on the sea shore 269

VIU

ED I TO R S' PREFACE

An object of the New Naturalist series is the recognition of the many-
sidedness of British natural history, and the encouragement of unusual
and original developments of its forgotten or neglected facets. One
such facet is the study of parasites, a study all too long regarded as
curiosity about mere curiousness, or as excursions into backwaters.
Some popular books that have been written on the subject have
stressed the unusual, the mysterious, often the macabre. Few have
taken the subject truly seriously. This book, which is at the same time
an able (and entertainingly written) popular exposition, and an original
and new scientific synthesis, will put things in a new and true
perspective.

"Birds," the authors quote from A. E. Shipley, "are not only birds
but aviating zoological gardens." This book is the first guide to those
gardens: it is the study of a community of animals, plants and bacteria
that is just as real, as any of the communities of the wood, the stream,
the field, or the sea. For the outside and inside of the body of a bird
(or for that matter, any other vertebrate animal) harbours, and
shelters a vast population of organisms, of many species, whose way of
life, relationships and importance are little-known and poorly under-
stood.

Birds are the most intensively-studied animals in the world-
yet only a few naturalists consider the existence of the birds' relation-
ships with the vast network of organisms that comprises their parasite-
community. Only a mere handful is interested in the subject. But
because birds are otherwise so well-studied, they make the best
starting-point for a development of the picture of parasites alive and
at work. It was fortunate for the New Naturalist that this view had
been held for many years by the two able workers whose researches
and wide scholarship have here borne fruit.

This book, then, leads the reader to the lessons to be learned
from the life of parasites, via the particular parasites of birds. To

EDITORS PREFACE

restrict the subject in this way forces a selection from a plethora of
examples (of which many are of the same kind) : but it does not result
in the loss or omission of any important general conclusions.

This is the first book devoted entirely to the various groups of
parasites which live in or on birds. It describes not only the mutual
impact of parasite and host, but the extraordinary modifications of
the parasites' sexual habits, life-cycles and anatomy which are associ-
ated with their loss of independence. The authors also touch upon
other curious relationships — between birds and Hymenoptera (wasps
and ants), birds and whales, birds and cattle, birds and cuckoos,
birds' nests and insects and mites.

Miriam Rothschild is a member of the famous family of mer-
chant bankers, and a sister of the present Lord Rothschild, who is
also a prominent zoologist. Like her late father, the Hon. N. Charles
Rothschild, she has always regarded parasitology as an hobby, but
has approached it scientifically. Since taking her zoological
training at London University she has carried out much experimental
work at the Marine Biological Station at Plymouth. Of about sixty
scientific papers that she has published, at least forty deal with para-
sites. She is probably the world's greatest authority on bird-fleas.

Theresa Clay, for her part, is probably the world's greatest auth-
ority on bird-lice and has published over forty scientific papers on
the subject. She has travelled widely accompanying scientific ex-
peditions to Africa, Arabia, Pakistan, North America, Iceland, and
the European Arctic. Like Miriam Rothschild, she is a trained zoologist
— a graduate of Edinburgh University ; and is now a member of the
stafif of the British Museum (Natural History).

Fleas J Flukes and Cuckoos points to many interesting fields for research.
All New Naturalist books tend to synthesise our knowledge of a
subject, to demonstrate deficiencies in that knowledge, and to
point to new goals. In this book the unsolved problems advertised, and
the new avenues charted but unexplored, seem to us to be more
numerous than in any other that we have so far had the pleasure
of editing. There is not even one worker in Britain who is
wholly occupied with that extraordinary group of animals, the
trematodes or flukes. If this lucid, informative and interesting book,
so unusually illustrated, does not stimulate a new surge of research
it will be no fault of the authors, and no credit to British
naturalists. The Editors

AUTHORS' PREFACE

Throughout this volume an attempt has been made to keep the
parasitic relationship in the foreground. In Part I we have dealt with
the more general aspect of the subject, and in Part III a brief survey is
given of the various groups of parasites which attack birds in Great
Britain. In Part II we have tried to present a close-up of two contrast-
ing types of parasitic insects, the feather lice and fleas, in order to
illustrate in greater detail the intimate relationship which exists between
host and parasite.

The ground we have had to cover is extensive. Some of the groups
of bird parasites contain hundreds of species of which many are well
known to specialists but are not yet described or named. In the fleas,
louse-flies, ticks and tongue-worms only, four exceptionally small
groups, we have been able to give a complete list of the species recorded
from British birds. In other sections, notably the worms, mites and the
fauna of nests, we have merely skimmed the surface of the subject. In
those classes in which the existing classification is considered un-
satisfactory and probably of a temporary nature only, references to
sub classes and orders have been avoided as far as possible. In this
edition (third edition, fourth impression) space has not permitted
alterations in the text, but merely the correction of errors and mis-
prints, and we have included some new and very important references
in the bibUographical appendix. We have also tried to keep the four
small groups mentioned above up to date by noting the recent addi-
tions on pages xiii to xiv. We have attempted to define "parasitism,"
"commensalism" and "symbiosis" in the text. The American Society
of Parasitology's Committee of Terminology decided that "the present
confusion necessitates the definition of the term [symbiosis] whenever
it is used" and we think this is true of all three terms. We should,
however, like to draw the reader's attention to the rather different
definition of these terms by authors such as Davenport (1955) and
Allee et al. (1949). In order not to overburden the text with "Latin"

authors' preface

names we have assumed that the reader is familiar with the popular
names of British birds, and have included their scientific names in the
index only. We have followed the classification and nomenclature in
Witherby's Hajidbook of British Birds (i 938-1 941).

Unfortunately it is quite impossible to name all those who have
personally assisted us in the preparation of this book or to refer by title
to the extensive literature we have consulted. In the chapter on fleas
alone we have quoted from over a hundred papers. We should never-
theless like to express our special gratitude and sincere thanks to all
those who have supplied us with specimens, information and criticism,
and to all the photographers and draughtsmen who have contributed
to the illustrations in this volume. Mr. A. L. E. Barron in particular
has lavished infinite care and skill upon the execution of thirty micro-
photographs which, in many cases, presented great technical difficulties,
and Mr. Arthur Smith has produced the excellent black and white draw-
ings. We should like to thank the Editors of the Proceedings of the Zoological
Society of London, for permission to reproduce Plate XXIV, and the
Editors of the New Naturalist series themselves for all the trouble they
have taken on our behalf. Mr. Eric Hosking took the magnificent
photograph of birds crowding on the sea-shore (Plate XL) especially
for this volume — a photograph which has already become famous.

M.R.
T.G.

September, ig^g

Xll

ADDITIONS TO THIRD EDITION

Chapter 7: Fleas (Aphaniptera).

The hen stick-tight flea {Echidnophaga gallinacea) has been recorded by

Thompson (1952) on a migrating White Wagtail {Motacilla a. alba) a bird

which winters in Africa, captured at Skokholm Island. (See pages 71,

84 and 108).
Waterson left out of his count 40 aberrant females (Smit, 1955), ^^ there

were actually 2,408 (59^0) females to 1,672 (41%) males. (See page 79,

line 21).
It is now considered (Smit & Allan, 1955) that C.farreni in North Africa is

only a variety. A distinct subspecies, however, occurs in Japan and

China. (See page 85).
C. riparius has now been found in Transbaikalia (Smit & Rothschild, 1955),

which suggests that it spread to the U.S. from the west. (See page 89).
Recently C. borealis has been found in moorland districts on the mainland

of Britain, and several cases of hybrids between it and C. garei have been

recorded from this habitat. (See page 89, map 2.)
Ceratophyllus lunatus has now been found in the nest of Anser leucopsis in Green-
land. (See page 95).
Ceratophyllus styx has recently been split into two subspecies, both of which

occur in Britain, C. styx Rothschild 1901 and C. styx jordani Smit 1955.

Hybrids are produced where the two suspecies meet. (See page 113).
Ceratophyllus vagabuna insularis has recently been recorded in Belgium. (See

page 115).
Chapter 9: Protozoa.
Baker has recently (1955) found a Plasmodium, probably P. relictum,m

three rooks, a jackdaw and a blackbird in Hertfordshire. (See page 165).
Baker ( 1 955) has recorded five species of Leucocytozoon from birds in Hert-
fordshire, namely L. majoris, L. sakharoffi, L. marchouxi, L. dubreuli and

L. danileuskyi. (See page 169).
Recently Baker (1955) has discovered thsit TrypanosojJia avium is transmitted

by the louse-fly Ornithomyia aviculariaj in which it undergoes cyclical

development in the gut. Birds become infected by ingesting infective

louse-flies. (See page 172).

xiii

ADDITIONS TO THIRD EDITION

Chapter ii: Louse-flies (Hippoboscidae).

Ornithomyia lagopodis is now considered as a synonym of Ornithomyia fringillina

(See page 213).
There have been two additional records oi Lynchia albipennis {= Ornithoponiis

ardaea) from Britain: one from the little bittern {Ixobrychus m. minutus),

and the other from the bittern {Botaurus s. stellaris). (See page 214).
There is a record of one specimen of Olfersia spinifera from a stray Man O'

War bird in the Inner Hebrides in 1953. This is a host-specific parasite

of the Fregatidae. (See page 214).
Chapter 12: Ticks (Ixodoidea.)
Ixodes passericola is also recorded from blue tits, great tits and a few other

species, and there are two records of Haemaphysalis cinnabarina from a

mistle- thrush and a skylark. (See page 231).
Chapter 13: Microparasites.

Poulding has recently recorded five cases of Aspergillosis in sea gulls in
Britain. (See page 243).

XIV

PART ONE

INTRODUCTION

Then said they, What shall be the trespass offering which we
shall return to him? They answered, five golden emerods,
and five golden mice, according to the number of the
lords of the Philistines : for one plague was on you all and
on your lords.

I Samuel 6

THE CHILDREN OF ISRAEL kncw that the bubonic plague was intimately
connected with rats. Indeed, a profound and intensive study of the
Bible might well have prevented, or at any rate reduced, the ravages
of the Great Plague of London. There is no hint, however, that the
ancient Hebrews were aware of the sinister role played by the rat
fleas, which, by their promiscuous feeding habits, spread the plague
bacillus from rodent to rodent and from rodent to man. The writers of
the Old Testament concentrated on essentials and, in this case, were
entirely justified in focusing their attention on the rats and mice them-
selves, for they are the true hosts of the bacillus in question.

To-day, in studying bubonic plague a large section of parasitology
and many of its related problems must be considered. A detailed
knowledge of the parasitic bacteria which cause the Black Death in
rats and, secondarily in man, is, of course involved, but it is also
necessary to study associated animals such as fleas, which act as carriers
and spread the disease, as well as a whole series of complex factors,
like climate, food and the habits and behaviour of the living organisms
involved. At one end of the chain we are concerned with the minute
differences in the sex organs of fleas and at the other with the inter-
national grain commerce of man.

a FLEAS, FLUKES AND CUCKOOS

The complicated relationship between parasites and their hosts is
one of the chief lures of parasitology. As children we puzzled over the
old woman who lived in a shoe, but such a situation appears common-
place compared with that of the worm which lives exclusively under the
eyelids of the hippopotamus and feeds upon its tears. To us, at any
rate, the parasite's existence seems strange — whether we are concerned
with a threadworm which passes its time partly in a bird's heart and
partly in an insect's mouth, or a bed-bug which hides in cracks and
crevices, and at night steals out to suck blood surreptitiously from a
sleeping beauty's breast.

It is only during the past hundred years that parasites, in their role
as carriers of disease, have stolen the limelight. It is now quite usual to
regard insects and ticks as the makers of history, the moulders of man's
destiny and as one of the real enemies of the human race. It was
possible to see and hear Hitler and Goebbels but it is impossible to
perceive the plague bacillus spreading poison or the malaria Plasmodium
bursting open red blood corpuscles. The small size of many parasites
makes them rather difficult to study. In order to find out something
about them it is necessary to spend a considerable amount of time in the
laboratory observing minute structural differences between one animal
and another with the aid of a microscope, and searching for small and
elusive stages of their life-cycle. This work can be both time-consuming
and extremely tedious, although at other times it can be exciting and
even dangerous — " Image of war without its guilt."

The most difficult problem to contend with in writing a book of this
sort is the fact that most parasites are obscure animals of which the
majority of field naturalists know little or nothing. If we analyse the
reasons why any particular natural history book strikes us as "very
good" we generally find that it has increased our knowledge of a
famiHar and well-loved subject. Ford's book on butterflies is an excellent
example of this kind. There is nothing new in this observation, for
everyone is aware that gossip about strangers is dull, whereas gossip
about one's friends is highly delectable. There is a tendency in all
human beings, however, to laugh at the discomfiture of others. The
thought of a tapeworm as long as a cricket pitch living secretly in the
stomach of a film star, or a beetle quietly chewing the feet of a close-
sitting hen arouses in us a feeling of macabre amusement. This is,
perhaps, fortunate, for it does not matter what initiates the naturalist's
interest, so long as it is aroused. Soon interest leads to familiarity and,

INTRODUCTION

in this case, familiarity breeds love. Many helminthologists find the
diffuse kidneys of intestinal worms not only profoundly interesting but
objects of considerable beauty. But this, like the aesthetic pleasure
derived from pictures painted by Picasso, although real enough, is an
acquired taste.

Birds are no more victimised by parasites than any other class of
vertebrates but, except for the fish Hce (Copepoda) and a few other
exclusively marine animals, they are attacked by representatives of
most of the well-known parasitic groups, ranging from unicellular
Coccidia to the more familiar cuckoos.

The ordinary "normal" bird supports a large number of both
relatively harmless and harmful parasites (see fig. i), the presence of
which is largely unsuspected by naturahsts as a whole. In fact, it
comes as rather a shock to the ornithologist as well as the bird lover to
discover the ills to which avian flesh is heir.

Their feathers are eaten and sometimes completely destroyed by
lice and mites. The superficial layers of their skin and its waxy exuda-
tion are devoured by certain flies. Mites and tongue-worms also
invade the nasal cavities, the bronchial tubes, air sacs and lungs and
feed upon their secretions. Fleas, hce, mosquitoes, midges, bugs,
leeches and ticks suck their blood from outside. Protozoa (one-celled
organisms), such as the malaria parasite, destroy the red blood cor-
puscles from inside the body. Other Protozoa, the trypanosomes,
are found in the bone-marrow and lymph vessels, and flagellates
swarm in the crop and mouth. Varieties of worms are located in almost
every organ of the body, the subcutaneous tissues, the muscles, the
eye, the brain, the trachea, liver, kidneys, gall-bladder, bile-duct,
reproductive organs and the ahmentary canal. Leeches fix themselves
inside the vent and sometimes in the throat-pouches of pelicans.

Moreover, there is not only a large variety of species of parasites
which can attack birds, but sometimes very large numbers of one sort
of parasite are found in a single individual. Thus, over 10,000
nematode worms are recorded from the intestine of a grouse and more
than 1 ,000 feather lice from the plumage of a single curlew. Shipley
was so impressed by the variety and number of their parasites that he
exclaimed, " They are not only birds but aviating zoological gardens."
The life history of the malaria parasite of man, perhaps the most
important discovery in the whole field of human parasitology, was
worked out on a closely related species from wild birds. The hfe-cycle

FFC— B

4 FLEAS, FLUKES AND CUCKOOS

of the human blood fluke, which was a serious plague throughout the
Middle East, could easily have been elucidated in this country and
much time and effort saved if we had made use of the similar type of
worm found here in the veins of ducks and gulls. From the utilitarian
biologist's point of view it is difficult to over-estimate the importance
of studying parasites. Birds which harbour many species closely
related to those normally infesting man render us a silent but in-
estimable service by their sad experiences. Most of the successful anti-
malaria drugs are first tried out on canaries.

From the naturalist's point of view, which is necessarily a rather
different one, parasites are equally important. Broadly speaking, the
public are no longer interested in evolution. The man in the street,
who has survived two world wars, together with mustard gas and the
atomic bomb, now accepts the suggestion that he is descended from the
apes without either indignation or surprise. Evolution has, however,
remained the lodestar of our generation of naturalists, and parasites are,
perhaps, the organisms in which evolution is most obvious. Their mode
of life has imposed certain definite morphological and physiological
modifications upon them — a sort of gigantic secondary experiment in
evolution, which, if properly studied, must prove profoundly illuminat-
ing. Moreover parasites act as pointers and guides to the evolution and
relationship of their hosts. Between these two an eternal and curious
struggle is in progress. The host's reactions are wholly hostile but the
parasite is forced to adopt a compromise. It has to restrict its activities
in such a way that it does not immediately endanger the host's life and
thus jeopardise its own food supply and chances of reproduction.
Parasites which neither stimulate the host to violent reactions nor
inflict upon it serious permanent injury are said to be "well adapted"
to their mode of life.

There are in nature certain associations in which the organisms
concerned suffer no ill effects and, on the contrary, are assured either
unilateral or mutual benefits. These relationships, which are known as
commensalism, symbiosis, and phoresy (see p. i8) may represent
transitional stages in the development of the parasitic habit. Some
hold the view that they precede parasitism. Others, with a more
ideahstic outlook, consider that adaptation has here evolved beyond
the parasitic relationship, with the ehmination of harmful effects and
a gradual substitution of mutual benefit. Whatever the truth may
be it is clear that a study of the borderhne associations is of consider-

INTRODUCTION 5

able importance if we wish to understand the parasitic relationship
itself.

It is, of course, a truism that all living organisms are inter-dependent,
but the origins and development of that acute dependence displayed by
parasites and commensals has a special fascination. At one end of the
scale there is a rove beetle which can apparently only breed in birds'
nests where the temperature is raised to about 40 degrees centigrade
by the presence of nestlings and, at the other end, the cuckoo, which
has also to seek out the nests of small birds in which to lay her eggs.
Once on the track of this sort of relationship, the naturalist becomes
more and more curious. He just has to go on.

•^ •^:^:y;V^^P^^^^

...1^

lllt^v?'^'

Bird-bottle fly, Protocalliphora azurea, resting upon
a flower (x 4.7)

CHAPTER I

PARASITISM

Almost
All the wise world is little else, in Nature,
But parasites and sub-parasites.

Ben Jonson

THE WORD parasite means, literally, one which eats beside another,
but the modern biologist cannot accept this as a definition. It is too
elastic and too vague. The term is now generally used to indicate
strict dependence between two organisms, one of which, at any rate,
during some period of its life, lives at the expense of the other. The
word parasite is often used in a broader sense to mean any animal or
plant which is dependent upon a host — and it is left to the reader to
decide for himself how exactly to define the term host.

Ultimately all animals depend on plants or other animals for their
source of energy. They must eat to live. Plants may subsist on an
ethereal diet — largely air and water flavoured with sunshine — but
animals require more substantial if less romantic fare.

Many biologists see in a parasite a form of predatory animal.
Instead of killing and devouring its prey whole, it can, by virtue of its
smaller size, live on the host or in it, and eat it little by little. The robin,
for example, has a number of relatively large carnivorous enemies such
as hawks, cats, rats and stoats which prey upon it and devour it whole.
It also supports a far greater number of animals smaller than itself
(Fig. i) which are parasitic and live by gradually eating relatively
minute portions of its body. Elton has described the difference between
a carnivorous and a parasitic mode of life simply as the diflference
between living on capital and income. If, however, an animal becomes
a parasite, the problems which confront it and the consequences of its
mode of life are unquestionably dififerent from those of a free-living

R. McV. Weston

a. Starling louse clinging to feather ( x 29)

Plole I

h. Quill louse inside wing-feather shaft of curlew ( x 23)

Plate II

Eric Hosking

Great spotted woodpecker: the parasitologist can provide a valuable clue to the
classification of this group of birds

PARASITISM 7

animal. Possibly there is some justification for those biologists who
consider these two habits of life — which are found everywhere and
which have been evolved as part of the general struggle for food and
shelter — as fundamentally distinct.

In nature we find extremely varied and diverse types of parasitism.
It is an easy matter to point to a louse and say with confidence, "There
is a parasite." It is equally obvious that a golden eagle is a bird of prey.
On the other hand it is difficult to decide if certain larval water beetles
and leeches, which sometimes kill and eat their prey outright and at
other times merely abstract a little fluid from living victims, are
carnivores or parasites. It is also obvious that there is a wide gap
dividing the type of parasitism displayed by a worm which lives
permanently in the veins of a sea-gull, immersed in a perpetual food
bath of blood, and a female gnat which occasionally visits the gull,
punctures its skin and withdraws a few drops.

Certain of these animals are described as obligate and permanent
parasites. The Protozoa which cause avian malaria, the tapeworms and
the feather lice, for instance, are compulsorily parasitic throughout
their lives. Tapeworms and Plasmodium live inside the bird (endo-
parasites), feather lice on the outside (ecto-parasites), but they are
always dependent upon their hosts and cannot live apart from them.
For these parasites, prey and environment merge and become one.

Although so-called obligate parasites are at some period of their
lives dependent upon a host, many of them are able to spend long
spells in the free state and it is normal for them to do so. Ticks gorge
themselves with blood and then drop off the birds into their nests or on
to the ground and remain there until they have digested the meal.
Bugs hide in cracks and crevices or in the deeper layers of the nest
during the day, but steal out at night and feed upon their roosting host.
Leeches drop back into the water after engorging around the mouths of
cattle and horses drinking in ponds or streams. These animals are gener-
ally referred to as periodical parasites, whereas those which are dependent
on a host during one stage of the life-cycle only, are designated as tempor-
ary parasites. A good example of the latter type is a beautiful metallic fly
{Protocalliphora azurea) which as an adult insect hovers over flowers in the
sunshine and sips nectar and dew, but as a larva lives by sucking the
blood of nestling birds. Another fly, Camus hemapterus, is parasitic as an
adult but the larva is a scavenger and dung-eater in the nest. Many
Diptera (flies) can be included in both categories. Gnats, midges and

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PARASITISM 9

blackflies are only parasitic in the adult stage and they too only visit the
host at irregular intervals, some by day and some by night. Very little is
known about the biology of these species and it is not quite certain
whether all are true obligate parasites. Some may be more correctly in-
cluded in the group of animals classed 2iS facultative parasites. These can
live and complete their life-cycles as free animals, but resort to para-
sitism if circumstances are favourable. For example, certain fly larvae
which normally hve on dead and decaying matter in nests are attracted
to any sores which may be present on the bodies of the young birds. They
may invade these areas and from then onwards f.ed upon the exudations
and the putrefying flesh in the cavity of the wounds.

There are also very large numbers of organisms which can be
called accidental parasites. Certain Protozoa, maggots and worms are
over and over again accidently ingested by birds and other animals
and can survive for varying periods. They feed upon secretion or even
hving body tissues although this is in no way their normal mode of life.

Among these groups we recognise many degrees of dependence,
diflferent and contrasting life-cycles and great variation with regard to
the mutual reactions of host and parasite. The feather lice and mange
mites, for example, which are so-called permanent obligate parasites,
pass generation after generation on the same individual animal, even
their eggs being attached to the outside or buried within the tissues of
the host. On the other hand, certain worms and many of the Protozoa
pass through tw^o or more hosts and, certain phases of their lives
present a great contrast, part being spent in warm- and part in cold-
blooded animals. Again, the tgg stage, or the spore and cyst stage,
of obligate parasites often passes from the host into the outside
world, and is the means by which another animal is reached and
the life-cycle recommenced.

Perhaps the most fascinating form of dependence among bird
parasites is what is now defined as brood parasitism. The feeding and
rearing of the young is entrusted to a diflferent species of bird. This
type of behaviour is not uncommon in the animal kingdom as a whole
but it is very rare among vertebrates. Established brood parasitism in
mammals is unknown, although in isolated instances and under dom-
estic conditions certain species will voluntarily rear the young of others.
The European cuckoo is the best known type of brood parasite among
birds and the only one found in Britain. It is an obligate parasite,
incapable of rearing its own young. There are, however, numbers of

FLEAS, FLUKES AND CUCKOOS

birds, apart from the cuckoos, which practise brood parasitism, to a
greater or lesser degree. The cow-birds (Icteridae) of America, the
honey-guides (Indicatoridae), and certain weavers (Ploceidae) especial-
ly the widow-birds of Africa, adopt a similar mode of life.

Not all these birds are as harmful to their hosts as the European
cuckoo, for in several species the foster parents rear the intruder as well
as their own young, which is left unmolested in the nest along with
the rightful owners.

Some birds, of which the skuas (Plate XXXVIIIa) are good examples,
live by a curious form of food robbing known as clepto-parasitism. They
are large and powerful birds, capable of killing their prey in the usual
predatory manner, but instead they prefer to chase other sea birds and
by their relentless attacks force them to drop the prey they have
captured or to disgorge their last meal.

Obligate parasites, facultative parasites, temporary or permanent
parasites, brood parasites, clepto-parasites, endo- or ecto-parasites —
all these categories have been invented by us for our own convenience
in order to simplify the task of description and exposition. They are
arbitrary classifications which do not bear critical analysis, and in
nature these types are found to merge gradually into one another.
Moreover, it is true to say even when closely related species of both
host and parasite are involved, no two parasitic relationships are
exactly alike.

Fungus, Aspergillus fumigatus {x 293),
a facultative parasite in the lungs of birds

CHAPTER 2

COMMENSALISM

And thou shalt eat bread at my table continually.

II Samuel 9 : 7

IF TWO animals live in close and harmless association with one another,
from which circumstances only one partner derives benefit, the
relationship is known as commensalism. Although widespread through-
out the animal kingdom, this somewhat mysterious phenomenon is
rarer than parasitism and not so easily recognised. If both associated
partners receive an advantage the relationship is known as symbiosis.
The most usual form of commensaHsm is one in which the smaller
and weaker of the two animals steals a Httle food from the larger
animal without causing it any appreciable loss or inconvenience. Thus,
a small species of muscid fly accompanies large blood-sucking clegs
(Tabanidae) and laps up a httle of the blood which may be left oozing
from the wound on the victim's skin. Although strictly speaking the
term commensal should be apphed to mess-mates only, in many such
associations the benefit received is one of shelter and indirect protection
from enemies rather than nourishment, while in others both these
advantages are conferred simultaneously. A minute worm, for example,
lives relatively safely in the groove on the arms of certain starfish and
when the host is feeding it wriggles up to the vicinity of its mouth and
surreptitiously catches a few stray morsels. In this way it obtains free
board and lodging. A more famous association exists between the
remora, or sucking-fish and whales and sharks. The remoras attach
themselves to the undersides of their giant companions by means of an
adhesive disc on their heads and thus obtain transport, protection and
any superfluous food accidentally dropped or discarded in their
vicinity. They also enter the gill cavities and mouths of large bony

12 FLEAS, FLUKES AND CUCKOOS

fish such as sword-fish and sun-fish and are carried about with them,
Hterally taking the food from their mouths.

In most cases of commensaHsm it is easy enough to see why the
active beneficiary cHngs to the association, but it is far more difficult to
understand why the passive partner tolerates the other's presence. One
is sometimes tempted to beheve there must be a psychological explana-
tion which cannot be observed from the outside.

For instance, a man from Mars would find it a simple matter to
understand the relationship between a shepherd and a sheep dog, or a
hunter and his hounds. On the other hand, he might well be puzzled
at the seemingly one-sided benefits enjoyed by pekinese and pug-dogs.
At present no one is in a position to say whether or not the starfish
receives agreeable sensations from the worm wriggling up its ambulacral
grooves. Is it possible that a remora, twitching in their buccal cavities,
assuages feelings akin to loneliness and boredom with which the sun-
fish and sword-fish are otherwise afflicted ? We do not know.

On the whole commensal relationship among birds is unusual and
when it does occur it is chiefly limited to the breeding season. It is,
however, common knowledge that many species of birds associate in
flocks, especially for feeding and during migration. The significance o
most of these associations — if indeed they have any special signific-
ance— is completely unknown. In the case, however, of wigeon and
brent geese, which are often seen together at their feeding grounds,
the duck can be described as commensals, for on such occasions they
feed on the debris of eel grass [Zoster a) which the geese have pulled
up and broken into convenient lengths. Nevertheless, the wigeon
are quite capable of breaking up the ^ostera themselves if there are
no geese about. In Lapland, waxwings have been seen feeding on
the berries of mountain ash, and scattering a quantity of pulped fruit
on the ground below. There, flocks of redpolls were waiting to
eat up the debris. They appeared unwilling to feed on the whole
berries and followed the waxwings from tree to tree. In south east
Africa, Swynnerton has watched swallows and bee-eaters accompany-
ing a party of bulbuls (Pycnonotidae) which were feeding on ripe
guavas. They were catching the insects accidentally disturbed by
the bulbuls.

In more familiar surroundings a casual commensal relationship may
be observed between the robin and the mole. As the mole tunnels just
below the turf and throws up fresh soil in the form of the familiar mole

COMMENSALISM I3

"hills" the robin watches intently from some convenient bush and
quickly seizes any invertebrates which are exposed on the surface.

Certain petrels and the great shearwater follow in the wake
of whales and porpoises and devour their faeces. In the South
Seas, the sheath-bills (Chionidae) enjoy a curious relationship with
various colonial nesting birds, which is part parasitic, part commensal
and part symbiotic. They haunt their breeding sites and steal many
eggs and scraps of food, but they also act as scavengers and obtain a
considerable part of their nourishment by eating the remains of
Crustacea found in the faeces of birds, especially of gentoo penguins
[Pygosceles taeniata). When the Weddell seals are bringing forth their
young the sheath-bills, like the ivory gulls in the arctic, will follow them
out to the pack-ice and feed on the placental blood and afterbirth of
the new born cubs. One observer saw several of them attempting to
eat the umbilical cord while it was still attached to the baby seal.

In Africa, the carmine bee-eater {Merops nubicus) rides on ostriches,
bustards and certain large mammals using them as perambulating
perches. It catches the insects which pass within reach of the "host"
or are stirred up in the grass. Once Myers saw a bee-eater fall off when
the bustard broke into a run but it flew after it and soon settled again.
This bird will also exploit bush fires fearlessly and darts in and out of
the flames to catch escaping insects. The native Mandigo name
means "nephew of the burning."

In the tropics there are numbers of spectacular examples in which
certain birds habitually nest in close proximity to dangerous social in-
sects such as ants, termites, bees and wasps. At first sight it would appear
that the benefit is always one-sided and while the birds obtain protection
from the presence of the insects, the insects themselves derive no advan-
tage from the association whatsoever. However, increased knowledge
about the birds concerned suggests that often mutual benefit is involved
and such examples will, therefore, be considered in a subsequent
chapter (p. 26). A case in which the insects appear to gain no advantage
at all concerns a South American parrakeet [Eupsittula canicularis) which
is an obhgate commensal of certain termites. It breeds exclusively in
their carton nests which it hollows out for the purpose. The parrakeet
never uses unoccupied termitaries, although plenty are available. When
building operations begin the termites rush to the scene of action and
try to repair the damage. They sometimes appear to make half-hearted
attempts to drive ofl^ the adult birds but they soon desist and leave them

14 FLEAS, FLUKES AND CUCKOOS

unmolested. They could easily kill the naked and defenceless young
when they hatch but, mysteriously enough, these are left unscathed. It
is obvious that the parrakeets benefit from the association. The termites
are irascible and their bite very painful. It is unlikely that egg thieves
would brave their fury in order to rob the parrakeet's nest. Moreover,
the termitary itself is hard and durable and also exceedingly warm.
Occasionally the adult birds even make a meal off their hosts. It is
certainly difficult to understand why the insects tolerate the presence of
these tiresome intruders.

There are also several species of woodpeckers, kingfishers and
parrots, in both the African and oriental regions, which are obligate
commensals of vicious ants and, like the parakeet, build, lay and rear
their young in the heart of the ants' nests. In one or two instances it is
known for certain that the woodpeckers habitually feed on the ants
concerned. The species of ants found in Britain do not lend themselves
to this type of association as they are not builders of carton nests. In
Sweden, however, Durango has seen three nests of the long-tailed tit
placed in close proximity to ant-hills of Formica rufa. On one nest the
wood-ants were swarming all over the outside. He observed that
squirrels avoided the areas where the ants occurred in large numbers.
This insect is a common species over a considerable area in Britain, and
where it occurs it is worth while keeping a sharp look out for incipient
associations between it and breeding birds — not necessarily the long-
tailed tit. It is generally species constructing domed nests which
establish such relationships with noxious insects, and the wren is there-
fore a bird to watch in this respect. The question of birds nesting
near bees and wasps in this country is considered in the following
chapter.

In various parts of the world small birds habitually build in close
proximity to some bigger bird, generally a bird of prey. Thus, for
example, the white wagtail regularly inhabits the nests of the osprey
and white-tailed sea-eagle on the coasts of Sweden and Finland. The
eyries of the prairie-falcon {Falco mexicanus) are frequently surrounded
by the clustered nests of cliff-swallows [Petrochelidon pyrrhonata). In
Africa some species of weaver-birds make a practice of grouping their
nests near that of an eagle, vulture or buzzard. A colony of nests of the
slender-billed weavers ( Teteropsis pelzelni) may be found actually hang-
ing from the sticks on the underside of a kite's nest. Among British birds
a rare vagrant, the red-breasted goose, and a winter visitor, the barnacle-

Ronald Thompson
a. Robin perched on spade: this bird is a commensal partner of man

*«. *

-V-

■^vt?

3^SSs^,::r^"-

A. Hen blackbird sunning: this habit may lead to the curious practice of "anting"
Plate IV

GOMMENSALISM I5

goose, arc known to seek the proximity of birds of prey at nesting time.
In Siberia the former species places its nest under cHffs occupied by a
pair of buzzards or falcons, which, it has been thought, assures the
geese some protection from marauding foxes. Another British species,
the red-necked phalarope, often seeks protection in its breeding haunts
in Iceland by nesting in close proximity to a sitting ptarmigan. The
ptarmigan is endowed with great courage and tenacity and drives off
the arctic skuas which otherwise persistently rob the phalaropes of both
their eggs and young. The wood-pigeon has also been observed on
several occasions nesting in the proximity of a breeding kestrel, sparrow-
hawk, merlin or hobby.

The last four examples are incipient but true commensalism, as the
benefits are clearly confined to the side of the defenceless bird. How-
ever, with colonial nesters such as the weavers it is rash to assume, as
most observers have done hitherto, that no advantage accrues to the
more powerful partner. It is possible that the weavers act as sentinels
for the raptorial birds with which they associate during the breeding
season. The rather curious biblical warning given to idle gossips may
have been based on some acute ornithological observation in the
field: " For a bird of the air shall carry the voice, and that which hath
wings shall tell the matter."

When the white wagtail breeds in the eyries of ospreys and eagles,
the association may also entail mutual benefit, for the wagtails have
been frequently observed and photographed hunting the insects in the
nests of their hosts.

Durango has collected numerous examples of birds which
apparently seek protection by breeding in the middle of colonies of
more aggresive species. In Sweden and Finland tufted duck and turn-
stone nest in gull and tern colonies — in fact there it is unusual to find a
nest of these two birds in any other situation. They even follow the
colonies if for some reason the gulls and terns change their breeding sites.
In Britain tufted ducks nest alone in concealed situations on the edge of
lakes and ponds. Long-tailed tits also frequently build in colonies of
fieldfares. On Faro in the Baltic, although typical and suitable nesting
sites in the form of sandy beaches are available, the little tern chooses to
nest in colonies of arctic terns on stony ground. In Sweden, France and
America the black-necked grebe breeds in colonies of black-headed
gulls, whiskered terns and Frankhn's gull [Larus pipixcan). The white
wagtail is a regular inhabitant of gull colonies on the coast of Finland.

l6 FLEAS, FLUKES AND CUCKOOS

Although these associations have not been adequately studied, probably
all of them will, in time, be recognised as commensal relationships.

There is another type of nesting association in which birds play a
popular and very prominent role in Britain. The erection of buildings
with clifT-like fa9ades, overhanging roofs and convenient eaves and
beams, has enticed swallows, martins and swifts away from rocky caves
and mountain precipices. It has brought them to live and breed in
close proximity to man himself. In Africa certain swifts and swallows
normally confined to breeding in cliffs which are by no means common,
have taken to nesting on buildings of European type — not only on
houses but also under bridges and similar structures. Their numbers
have since greatly increased. It seems likely that a similar course of
events occurred in Britain. Probably at some remote period both man
and martins shared the same caves and cliffs around the coast, and the
birds eventually followed man and made use of his new and self-made
habitations.

The poets have described the difference in the nesting habits of the
various members of the swallow tribe. In England "the temple-haunt-
ing martlet" seeks out the purely human dwelling more persistently
than the swallow. It favours baronial halls, castles, small towns and
villages where it "builds in the weather on the outward wall." On the
other hand the swallow "twitt'ring from the straw-built shed" prefers
the company of domestic animals. The arrangement of beams and
roofing inside farm buildings is better suited to its nesting require-
ments.

Swallows show a slight preference for certain domestic animals.
Their prime favourites are cows. Other things being equal they will
build in an occupied cowshed rather than a stable or a pigsty, although
their love of pigs and horses is also great. Sheep are not so acceptable
as companions.

Human beings obtain great delight from the presence of swallows
and martins which nest on their barns and houses. They are not only
intrinsically beautiful and graceful birds, but since they arrive in March
and April they have become the symbol of spring flowers and sunshine,
and the nostalgic hope of better times to come. Man, however, is for
ever seeking utilitarian motives for his actions. We find, therefore, that
various "reasons" are put forward why the birds should be actively en-
couraged. It is frequently asserted, for example, that swallows rid the
cowshed of noxious and irritant flies. There is also a widespread

GOMMENSALISM I7

superstition in Britain that if the swallows' nests are robbed of eggs the
cows give bloody milk. So far there is no evidence that man benefits,
either indirectly through the well-being of his stock or directly, except
aesthetically, from the close proximity of the birds, and any advantages
appear entirely on the side of the martins and swallows. Nevertheless,
if we admit the psychological element it is evident that the relationship
entails mutual benefit.

Much the same may be said of the curious ties that link the robin
and man in Britain. The bird receives all the tangible advantages,
which chiefly consists of food deliberately or accidentally provided during
the critical winter months. Man, on the other hand, obtains great
aesthetic satisfaction and pleasure from the bird's song and appearance,
but most of all from its tameness.

^' But what gives me most joy is when I see
Snow on my doorstep printed by their feet.''

In many other regions of Europe the robin is a shy woodland species
which shuns human habitations and is ruthlessly trapped, persecuted
and eaten by man. Fairly reliable figures show, for example, that
twenty thousand robins were killed for the table in one season near
Toulon in France. In England to-day a man known to eat robins would
risk social ostracism. Here we have the interesting phenomenon of two
species exhibiting a commensal relationship in one part of their geo-
graphical range and a predatory relationship in another.

There are several birds in Britain which enjoy less well marked
commensal relationships with man. Thus, jackdaws, rooks and gulls
regularly follow the plough, and sparrows, wood-pigeons, and stock-
doves obtain a considerable proportion of their food from agricultural
crops. In British seas and on the Newfoundland Banks the fulmar and
great shearwater follow the trawlers, and round the coasts where the
fishing vessels discharge their catches, various species of gulls are
commensals of fishermen. During the last sixty years many black-
headed gulls, herring-gulls and common gulls have changed their
habits in the winter. When the cold weather sets in they move up the
rivers into the large towns where they obtain food in the parks and
along the water fronts from the passers-by. These movements are
diurnal and towards evening the gulls can be seen flying away to roost
in quieter surroundings.

l8 FLEAS, FLUKES AND CUCKOOS

One of the most curious and unusual types of commensalism is
demonstrated by tits which have recently developed the habit of stealing
milk from the bottles left by the milkman on his rounds (See Plate III).
This remarkable phenomenon was first noticed about thirty years ago
in England and it has since spread rapidly through many parts of
Britain. Mainly great tits and blue tits, but also several other species,
rob the bottles and they systematically remove paper or metal caps to
get at the milk. Although this habit has undoubtedly arisen spon-
taneously and independently in different parts of Britain there is no
reason to doubt that its spread has been greatly accelerated by the tits
learning from their parents and by mimicking one another. It is a good
illustration of Elton's transmission of new ideas and new behaviour
which does not involve "any organic inheritance or mutation in the
ordinary sense." The kea's behaviour (see p. 23) is probably another
example of the same type of learning.

The word "phoresy" was coined to describe the passive transport of
one insect by another, but the term is now used to indicate any regular
association of this type, not necessarily between insects. Occasionally
phoresy and commensalism are difficult to distinguish and almost
merge into one another. In the case of remoras we know that the small
fish are not mere hitch-hikers but get free meals during their travels.
The larvae of certain mites (hypopus stage, Plate V), on the other
hand, which are carried about by a great variety of insects, and have
like the remoras developed special suckers for the sole purpose of
clinging to their transport hosts, have no mouth parts. Therefore we
can assume their journeys are no mere joy rides, but entail long fasts.
This is the classical type of phoresy — a highly specialised method of
dispersal with the object of finding new hosts. It is more difficult for
instance to define the relationships between those mites which destroy
the eggs and larvae of certain insects, and the adult insects upon which
the mites hitch-hike. The unsuspecting female carries them around
until she lays, whereupon the mites quickly terminate their trip and
transfer to the eggs, which they eventually consume. Certain curious
nest-dwellers, the pseudo-scorpions (p. 248) are great hitch-hikers and
use birds as well as insects as a means of transport.

There are a few curious records of snails being found in the plumage
— especially under the wings — of newly arrived migrant birds. Several
plover have been found with the same species of bladder snail {Physa)
both in the crop and among the feathers. It was suggested that these

GOMMENSALISM

birds might deliberately place snails in their plumage (see also p. 127
for a description of "anting") before starting on a long voyage in order
to provide themselves with at least one meal on the trip. Whether the
presence of these snails is accidental or not, it is certainly a method by
which their range can be extended — even to remote oceanic islands.
Even more extraordinary, and reminiscent of the ancient fable of the
eagle and the wren, is the record of a migrating short-eared owl trans-
porting a live goldcrest.

So far we have considered only those commensal relationships in
which the bird plays the active role, seeking either food, protection or
suitable nesting sites, or perhaps all three, from an indifferent or at
any rate acquiescent partner. The greater number of so-called com-
mensal relationships involving birds, however, are those in which
arthropods are the active partners (see Chap. 14). Birds' nests form an
ideal environment for these animals and within them insects and mites
teem in thousands. The chief benefit which the majority of these nest-
dwellers enjoy is no doubt the relative dryness and warmth of the
habitat. They have solved a very ancient problem : "Again, if two lie
together, then they have heat : but how can one be warm alone ?'

Moth, Tinea lafella,
a commensal from birds' nests (x 4.5)

FFC— c

CHAPTER 3

SYMBIOSIS

Now for as much as the Crocodile sojourneth in the water,
he hath his mouth all full of leeches within. Whensoever he
goeth up out of the water on the land, and thereafter yawneth
(which he is wont commonly to do when the west wind
bloweth) then entereth the Sandpiper into his mouth and
swalloweth down the leeches, and the Crocodile is pleased
at the help which he receiveth and hurteth not the Sandpiper
at all.

Herodotus

"HEN TWO different species of animal or plant live in close associa-
tion, from which they derive mutual benefit, the relationship is
known as symbiosis. A few biologists hold that the term implies
dependence and that its use should be restricted to those rare cases in
which neither partner can survive without the other. An assassin-bug,
[Rhodnius prolixus) and its symbiotic fungus [Actinomyces rhodnii) provide
a good example of this relationship. The fungus lives in the intestine of
the bug and is passed from generation to generation on the eggshells
and in its faeces which are then eaten by the nymphs when they hatch.
Without the fungus the insects' development only proceeds normally
until the fourth or fifth moult, and the majority fail to become adult.
The few which complete their metamorphosis are sterile and do not
reproduce. It is thought that the fungus provides a source of vitamin
B for the bug, essential to its proper development. At any rate the two
organisms are entirely dependent on one another for survival. The
majority of biologists, however, beheve that the word "symbiosis"
should not be interpreted too rigidly and can, therefore, be used to
describe any regular, though not necessarily obligatory, association in
which benefits are enjoyed by both partners. Thus, the world-wide
relationship between man and the cow is clearly symbiotic, although

SYMBIOSIS 21

there is considerable difference in the advantages which accrue to a
sacred cow of the tlindus and a British dual-purpose shorthorn.

A bird which may, with justification, be considered a symbiotic
partner of man is the barn-owl (Plate VI). It regularly makes use of
sheds, out-houses and barns during the breeding season and also
frequently roosts in buildings. In return it renders an invaluable
service by destroying large numbers of vermin which infest stacks and
farmyards. " It is as useful in clearing these places from mice,"
remarked Pennant, "as the congenial cat."

There is one family of birds, the starlings (Sturnidae), of which
several species have, independently in different parts of the world,
developed symbiotic relationships with the large grass-eating mammals.
The common starling in Britain supplements its diet by paying periodi-
cal visits to flocks of grazing sheep and cows and feeding upon the
insects which they stir up in the grass, or by actually picking parasites
off the animals' backs.

There are few prettier sights than a flock of starlings whirling out of
the frosty air — their wings transparent against a low winter sun — and
setthng among folded sheep, or a herd of cows. They work carefully
and painstakingly over the ground which has been disturbed by the
footsteps of the farm animals, and perform an extremely useful service
by destroying the disease-carrying ecto-parasitesofdomestic animals and
removing grass-eating insects and parasitic worms from their pastures.
The relationship is certainly of mutual benefit, but although quite
regular, it is essentially casual and each party can do quite well with-
out the other. The African ox-peckers [Buphagus], on the other hand,
obtain their entire food supply and much of their nesting material from
the bodies of the large herbivores and are thus wholly dependent on
wild and domestic animals. They have developed a very close relation-
ship with their partners, especially the rhinoceros, for which animal in
particular they act as sentinel. Big game hunters were the first to
appreciate this fact, for the birds frequently spoiled their chances
of a fine bag. "On many occasions," wrote Andersson, "has this
watchful bird prevented me getting a good shot at that beast ; the
moment it suspects danger it flies up into the air uttering sharp
shrill notes that never fail to attract the attention of the rhino-
ceros, which, without waiting to ascertain the cause, almost instantly
seeks safety in precipitate flight." Moreau has noted that the ox-
peckers, on occasions, stick very close to their "hosts", even clinging to

22 FLEAS, FLUKES AND CUCKOOS

the flanks of the greater kudu antelope (Strepsiceros kudu) galloping at
full speed !

It is a remarkable but not altogether agreeable sight to see ox-
peckers "working" over the bodies of large mammals. In some ways
they remind one of nuthatches or tree-creepers searching a tree trunk
for insects, for they flatten themselves against any perpendicular
surface and use their tails and feet in much the same manner. On the
other hand the ease with which they move backwards and forwards is
distinctly reminiscent of certain feather lice. They run and hop about
the beast they are "de-lousing" in a very lively fashion, diligently
searching every portion of its body, and we are told, "They often make
long drops downwards from the shoulder to the foreleg or down the
side of the animal whose coat they are engaged upon ... If alarmed
when at work on a giraffe's long neck they descend rapidly like a rat or
a mouse down the whole length of the anatomy of the beast and finally
come to earth by way of its legs ! If endangered by the sweep of the
host's tail they flatten themselves still more and allow it to brush
lightly over them, or jump nimbly out of the way." This habit of
continually rising and resettling on the host's body was also observed by
Moreau who was reminded unpleasantly of blow-flies round a carcase.
However, their attentions appear welcome to these large animals who,
far from being irritated by the birds' fidgety behaviour, even tolerate
them clinging and crawling about their faces and heads. Most observers
have been impressed with the apparent understanding which exists
between the two partners, for the bird's presence appears to convey a
sense of well-being to the mammals.

The crop contents of ox-peckers have been examined and their food
is found to consist mainly of ticks (an average of about forty ticks per
bird) and biting flies, although lice are also taken in smaller numbers.
In addition to ecto-parasites, clots of blood are frequently encountered
in the crops of ox-peckers, for they have developed the sinister habti
of eating the flesh and blood from the sores of cattle which they are
de-lousing. It is said that the birds do not inflict the wounds but merely
enlarge those which may already be present. They have, nevertheless,
in this way, become a nuisance to domestic cattle, particularly herds
which are in poor condition. The same tendencies are displayed by
the European starling in certain parts of the United States. Recently,
during an exceptionally cold spell of weather, when other sources of
food became scarce, the birds likewise began to eat the flesh wounds on

a. ( X 264)

J. G. Bradbury

-m^jnfc^m^eis, ^-"^^

Cw ■".»% ««.

b. ( X 230) Arthur L. E. Barron

PHORESY: THE HYPOPUS LARVAE OF MITES BENEATH THE SCLERITES

OF BIRD FLEAS
Plate V

'L. "'*. "-*»

Eric Hosking
Plate VI , _ , ^, .

Barn-owl feeding rat to young: owls are frequently infested with rodent Aeas and this
photograph illustrates how the transfer from mammal to bird can occur

SYMBIOSIS 23

the backs of cattle. In this case the initial puncture was said to be made
by the starlings themselves while enucleating the cysts of bot flies and
warbles which are located beneath the hide. In any case it is a short
step from enlarging an old wound to inflicting a new one. The keas
of New Zealand [Nestor notabilis) learned the bad habit of eating flesh
off the backs of sheep by the innocent practice of collecting wool for
nesting material. The situation is obviously fraught with great danger
for both the ox-peckers and starlings and should the balance tip
towards parasitism, the starlings' days, at least in the United States,
are numbered.

Apart from this bird there are several common British species which
feed fairly regularly if casually among domestic animals. Magpies,
jackdaws and rooks are not infrequently seen perched on the backs o
sheep, pecking off ecto-parasites and fly-larvae (see tail-piece Chapter
1 1) which are often located just beneath the skin. They also work the
grazing land for insects and parasitic worms.

An unusual type of "de-lousing" is carried out by the grey phalarope,
a tame, delicate little wader, which is a passage-migrant in Britain. It
frequently accompanies surface shoals of large fish and whales,
periodically alighting on their backs and removing and eating
their ecto-parasites. Aquatic animals are entirely at the mercy
of these gruesome creatures, which they acquire in the water
and are incapable of dislodging. Pliny noticed with sorrow that
"when fishers twitch up their hooks they see a number of these skippers
and creepers settled thick about their baits . . . And this vermin is
thought to trouble the poor fish in their sleep by night within the sea."
Most of us who have witnessed large fish landed in trawls or nets
experience a thrill of horror at the sight of the "lice" (Copepoda) and
worms plastered on their gills, around their sexual aperture and anus
and other tender and vulnerable areas of their bodies. The phalarope's
activities must be particularly welcome to whales and one wonders if
these animals dehberately rest on the surface with the object of attract-
ing their attention.

Historically the association between the crocodile bird and the
crocodile is the most famous symbiotic relationship ever recorded. A
translation of the well-known passage by Herodotus is quoted at the
head of this chapter. To-day there is no known bird which habitually
enters the mouth of the crocodile to de-leech its gums, although
Meinertzhagen has seen the Egyptian plover do so on more than one

24 FLEAS, FLUKES AND CUCKOOS

occasion. For all we know the species referred to by Herodotus as the
" Trochilus " may now be extinct. However, it is generally believed
that the Egyptian plover [Pluvianus aegyptius) is the species concerned
and it is to-day referred to as the crocodile-bird. It certainly pos-
sesses many of the attributes generally associated with birds mani-
festing this type of symbiotic behaviour. Its plumage is conspicuous, it
is unusually tame and according to at least one observer its flesh is
extremely unpalatable. All birds which habitually "de-louse" large
animals show a certain degree of tameness and boldness. This is
equally true of starlings, ox-peckers, phalaropes, mynahs, weavers and
magpies in the old world and grackles, tickbirds and cowbirds in
America. Moreover, the majority of birds which "de-louse" cattle or
associate with them on pastures are gregarious and go about in flocks or
small parties. One is inclined to think that only species which are in
some way protected against predators can afford to expose themselves
continuously and blatantly in the middle of open country on the backs
of cows or buffaloes. The flock definitely affords them some protection,
for birds of prey will often attack certain species if they happen to come
across a single individual but would not dare to do so if they are present
in numbers. Cott's recent work on the unpalatability of certain birds
suggests that the "de-lousers" are evil-tasting species which conse-
quently do not fear raptorials.

The buff-backed heron is a scarce wanderer in Britain, only two
specimens having been recorded with certainty from this country. In
its native haunts in southern Europe, Asia and Africa it is known as
the cattle-egret. This bird has developed a close relationship with
cattle, with which it associates in the fields, feeding on the ecto-
parasites which drop off them and the insects which the animals disturb
in the grass as they wander through the pastures. One of the most
interesting points about this partnership is the egret's predilection for
domestic animals and the way in which it has modified its habits to fit
in with theirs. In Africa in certain districts during the rainy season, the
cattle are concentrated in fly-free areas north of latitude lo and the
buff-backed heron moves up with them. In the dry season large
numbers of both animals again move southwards — the birds' local
migration being entirely dependent upon the cattle. At sunset the
domestic animals are confined in a compound and the egrets then
repair in a flock to a nearby swamp or lake. After drinking and bathing
they return to the village or cattle camp where they roost communally

SYMBIOSIS 25

in an adjacent tree. Unlike most herons they do not leave the roost at
sunrise but wait until cattle are released from the compound. As many
as sixty-eight cattle ticks have been taken from the egret's crop, but
they are by no means confined to this type of diet. Frogs and other
aquatic animals are taken freely if they come across them.

The only British breeding bird which takes advantage of the winged
insects swarming on domestic animals is the yellow wagtail which
hawks for blood-sucking horse-flies and clegs (Tabanidae) round cattle
grazing in the fields. Its vernacular name in France means "little
herdsman" and at least two African tribes designate it as "goatherd."
The degree with which these species of birds associate with cattle seems
to vary in different districts and even with different individuals. De-
lousers will often take advantage of any unusual circumstance which
disturbs insects from their hiding places. Thus cattle-egrets keep just
ahead of bush fires and mynahs follow sudden inrushes of water —
intercepting the insects which are disturbed by the flood and flames.
One species of ani or tick-bird {Crotophaga) has developed the interesting
and curious habit of following columns of the dreaded legionary ants
[Dorylinae) and feeding upon the insects which are "flushed" by the
ants as they drive relentlessly through the forest.

In south-east Africa Swynnerton has made a long and careful study
of mixed bird parties and has come to the conclusion that although
sociability and the protection of the weaker species concerned may
account in part for these flocks, their principal function is co-operative
hunting. They are in all probability drives. He has watched, for
instance, the different species in a mixed party searching the vegetation
at various levels, while others again such as drongos (Dicruridae) and
flycatchers moved along with them and only took insects on the wing
which were disturbed by the "beaters." The role of the drongos was
apparently that of clepto-parasites but Swynnerton surmised that their
aggressive nature and readiness to attack made them very welcome
additions, and no doubt greatly added to the "mobbing" force of the
whole party.

Little is known about the function — if indeed there is one — of the
various winter flocks of birds in Britain. It is not infrequent to meet
mixed parties of tits numbering a hundred or more. Recently it has
been shown that blue tits search trees and bushes at higher levels than
great tits, and it is quite possible that co-operative hunting is one of the
objects of these flocks. The association of feeding starlings and lapwings

26 FLEAS, FLUKES AND CUCKOOS

may also have some similar function. In any case it is a subject worthy
of further investigation in this country.

In the previous chapter we have described birds which seek
protection by building in or near nests of termites and ants. We must
now consider an even more interesting nesting association between
certain birds and Hymenoptera in which both partners are thought to
receive protection. In South America, to take one example, the yellow-
backed orioles {Cacicus cela) — brilliant yellow birds, very conspicuous
in every way — build in colonies around one of the great wasp nests.
They place their nests so close to the wasps that when the tree sways
the homes of the insects and the bird rattle against each other in the
wind. Their presence keeps off the principal enemies of the orioles,
such as egg-thieving opossums, tree-snakes and monkeys. It was Myers
who first pointed out that the birds in a lesser degree also protect the
insects. Any accidental damage suffered by wasp nests is likely to be
by animals which have failed to notice their presence until too late. The
intruder, needless to say, regrets the episode just as keenly as the wasps
themselves. Brightly coloured birds grouped about the nest serve as an
advertisement which warns all and sundry from a safe distance that the
wasps are there. In other words once the birds become well-known
recognition-marks of the ensemble they serve as an additional warning
mechanism. Moreover, most, if not all, colonial nesting birds — of which
rooks are a fair example — keep a sort of permanent lookout or watch,
and at the first intimation of danger the whole colony is in an uproar.
It is probable that the unusual noise and movement also disturbs the
wasps. To be forewarned is to be forearmed, and it is no doubt of great
value to the insects to be made aware of danger before it is at close
quarters. This gives them the opportunity of driving off the enemies
before they are within reach of the nest itself. In Africa, as well as in
South America, some of the birds — although by no means all of them —
which are concerned in similar associations are both colonial nesters
and very conspicuous.

It is only in fairly recent years that the nesting associations between
insects and birds have attracted much attention. The subject is excep-
tionally interesting and complicated and the reader is referred to the
original papers by Moreau and Myers listed in the bibliography. A
question which naturally occurs is this — do nesting associations of this
type, between wasps, bees and birds exist in Britain, which have hitherto
been overlooked ? The obvious place to search for such an incipient

SYMBIOSIS 27

relationship is near bee-hives in gardens. Birds which normally nest
around human habitations are gregarious and as we have already
noted, several species of birds and families of birds which manifest
general gregarious tendencies, seek protection from bees and other
social insects.

There are a few British records of birds nesting and rearing young
in close proximity to Hymenoptera.

(i) A jackdaw nesting two years running in a hollow tree with wild
bees — both birds and insects using the same entrance hole.

(2) A jackdaw nesting in a hollow ash tree with hornets — using the

same cavity but different entrance holes.

(3) A swallow and wasps nesting under the same eave, with the nests
touching each other.

(4) A sparrow and hornets nesting under a thatched roof situated about
one foot apart.

(5) A wren and wasps nesting within six inches of each other in an
attic.

All five birds reared their young successfully, which, in two instances,
were known to be second broods. These particular associations may
well have been accidental and due to a predilection for the same type
of nesting site. But this fact in no way detracts from the interest of such
records. Chance must play a very considerable part in first bringing
symbiotic or commensal partners together. Once such a partnership
between species has been firmly established, it is on the whole, fairly
obvious, although in the case of birds, recognition by naturalists in the
literature, came suprisingly late. On the other hand, in the early
stages before the relationship has become fixed as a specific habit,
individual cases are generally dismissed as coincidences. It is however,
unwise to disregard such isolated observations or dismiss them lightly.
Nothing is really known about the origins and evolution of nesting
associations between birds and aggressive insects or other species of
birds. Some workers believe it is merely a question of identical habitat
preference, or that the main element involved is the sociability of
birds. Others again consider that nesting sites close to an aggres-
sive species are less disturbed by predators and are therefore more
attractive to the birds. It is quite possible that all these factors play
a part and may wholly explain some of the cases concerned. Never-

28 FLEAS, FLUKES AND CUCKOOS

theless no really adequate theory has been produced to cover all the
facts relating to the close association between nesting birds and vicious
insects.

We have described how starlings destroy the ecto-parasites of cattle :
there are some mites and insects which perform a similar task for the
starlings. Foremost among these minute "de-lousers" is a group of
predacious mites, the Cheyletidae, which live permanently on the body
of birds and prey on feather mites (Analgesidae) and possibly also eat the
eggs of feather lice (Mallophaga).

In the previous chapter attention has been drawn to the fact that
many of the insect inhabitants of birds' nests are beneficial to their
hosts. Many rove beetles (Staphylinidae), some species of which are host
specific, are regular inhabitants of birds' nests and mostly prey on
insects or mites, including ecto-parasites. Certain fly-larvae and mites,
and a few moth larvae found in nests are coprophagous and feed on the
birds' excrement.

In tropical countries a true symbiotic relationship has been
developed between birds and certain flowering plants. Thus, hum-
ming-birds (Trochilidae) with their long slender bills and tube-shaped
tongues imbibe nectar and pollinate and fertilise the flowers as they
pass from bloom to bloom. Various species show a marked prefer-
ence for flowers of certain colours, especially scarlet, and the ruby-
throated humming-bird {Archilochus colubris) migrates northwards
across America and Canada as different red flowers open in succession.
The Honey Eaters (Meliphagidae) have an elaborate brush on the tip
of the tongue which acts as an efficient pollen-collecting device. In
Britain red berries attract birds and a much more casual and ill-
defined relationship exists between berry-eating thrushes, for instance,
and plants like the hawthorn and yew. The berries are eaten and
the fleshy portions digested, while the seeds which they contain pass
through the birds' bodies and are disseminated in a condition in
which germination can take place. In the plant world however, there
are copious examples of very strict dependence among symbionts.
A classical relationship is that between fungi and orchids. The seeds
of the latter cannot germinate without certain chemical substances
which are supplied by the former. The fungi on the other hand
can only live on the plants from which they derive their own nourish-
ment. Hence the relationship takes the form of a close and powerful
alliance, but there are rather similar associations in which the situation

SYMBIOSIS 29

can be better described as an armed truce. This state of affairs is also
encountered in the various commensal and symbiotic relationships
between vertebrate hosts and bacteria and Protozoa. As we have seen,
the host frequently tolerates the presence of commensals. Tolerance
in the opinion of Goodrich, is merely a stage between immunity
and disease. Symbiosis, Bernard has declared, is the frontier of
disease.

CHAPTER 4

THE EFFECT OF PARASITES ON THE HOST

If you join two lives, there is oft a scar

Robert Browning

*'r-r-iHE PEARLS of Britain," records Pliny, "be small, dim of colour and
J. nothing orient." But Julius Caesar openly admitted that the
breast plate which he dedicated to the Venus Genetrix was made of
English pearls. This may have been partof aCome-to-Britain campaign
designed to boost the Empire, but Pliny insinuates that the great
conqueror was mean and deliberately foisted second-rate pearls on the
Venus Mother.

These pearls were found in the shells of fresh water mussels. Scot-
land enjoyed quite a flourishing pearl trade as late as the reign of
Charles II and the rivers Tay, Don and Spey were particularly famous
in this respect. It is said that one very large pearl from Wales is mounted
in the British Crown. If so it forms a fitting monument to the extreme
hazards of the trematode worm's life-cycle.

Pearls in Britain to-day are found chiefly in the marine mussel
(Mytilus edulis) and not in the fresh water species {Unio and Anodonta),
They are usually formed round the body of a bird-parasite — a worm
which uses the mussel as an intermediate host and is found, in the adult
stage, in the reproductive organs of maritime ducks such as the eiders
and scoters.

The mantle of the mollusc, a flap of skin which envelops the soft
part of the body, secretes a hard substance popularly known as mother-
of-pearl, with which it forms the lining of the shell. If the parasites
become accidentally attached to the outside of the mantle, they are
quickly enveloped in a covering of epithelial cells. These cells continue
to secrete and to envelop the worms in fine alternating concentric

• ■ i

J. G. Bradbury
a. Section of pearl from freshwater mussel, River Tay ( x 20)

J. G. Bradbury
b. Goby infected with metacercariae of the herring-gull fluke, Cryptocotyle lingua ( x 1-3)
Plate VII EFFECT OF PARASITE ON HOST

a
o

bo
C

V
V

THE EFFECT OF PARASITES ON THE HOST 3I

layers of aragonite and conchiolin, thus forming the iridescent and
highly prized pearls. These rhythmical lines of growth are well
illustrated in the photograph of a section of pearl from the River Tay
in Plate Vila. Other intruders, such as mites or larval tapeworms or
inorganic matter, may also serve as the centre round which pearls are
formed.

Pearls and tuberculosis are both manifestations of the host's
response to parasites. They represent two extremes. The single
lustrous sphere in which the duck fluke lies entombed is the mussel's
successful solution of a relatively simple problem. The extreme
emaciation, suppurating liver and other gruesome symptoms of an owl
or a rook suffering from tuberculosis are, on the other hand, the bird's
desperate and ineffectual reactions to bacterial toxins which eventually
prove fatal.

The results of parasitism upon a bird are varied but generally the
harmful effects are brought about in a Hmited number of ways. The
parasites may consume the body tissues or body fluids of the bird, or
produce substances which are poisons or irritants. They may inflict
grievous bodily wounds or cause mechanical injury by pressure or
obstruction. They may bring about changes in both metabolism and
behaviour and, lastly, introduce other more deadly parasites into the
bird's body.

Sometimes one parasite can, at different times, affect the host in
all these ways. Leeches, for example, eat the blood of their bird host.
Their saliva is poisonous and may inflame the body tissues and even
kill the bird. The wounds they inflict while feeding do not heal easily
and severe haemorrhages frequently ensue. They also occasionally
suffocate the bird by crowding together and obstructing the air
passages. They are carriers of spirochaetes and fowl-pox.

Apart from the obvious consequences of these attacks by parasites,
obscure and indirect reactions are also involved. For example, the
herring-gull fluke, in its first larval stage, infests the common peri-
winkle (Plate XXVIIIa) and feeds upon its sex organs. It castrates the
host, thus first of all making further reproduction impossible for the
snail and also causing it to grow in size. The host is thus turned into a
giant eunuch. From a cursory glance at the outside of the shell a
practised eye can pick out any one of these sadly afflicted winkles.
They are specially favoured by fishmongers who, innocent of the reason
for their large size, display them prominently on their slabs and

32 FLEAS, FLUKES AND CUCKOOS

counters. Fortunately, in this stage both worms and winkles are
digested by the equally innocent customer.

The second intermediate hosts of the herring-gull fluke are various
kinds of inshore fish. The larvae penetrate beneath the scales and into
the superficial layers of the skin and there become encapsuled. The
tissues of the host react by producing a concentration of pigment round
the cysts. The whole fish then appears to be covered in an unsightly
rash of black spots. The common goby photographed on Plate VI lb
has been heavily infected with these larval trematodes. Such a heavy
attack as this, which results from a chance meeting with a dense swarm
of larvae, frequently kills the fish. The cercariae pour out a secretion
from the penetration glands to facilitate their entry through the skin.
This secretion is highly toxic if injected by thousands of larvae
simultaneously. To get some idea of what the fish experiences we may
imagine walking into a swarm of flying ants on a hot summer afternoon
and suddenly, all too late, realising that the ants have settled, cast off
their wings and are quickly boring into the skin. When parasites
attack human beings in swarms they are generally microscopic organ-
isms which are drawn passively into the body with air or swallowed with
food or water. Even those trematodes which will attack a swimmer and
actively penetrate the skin are so small compared with their victim
that at the time of invasion he is unconscious of the event. Sometimes
he may experience a mild prickling sensation of the skin and a fiaint
rash appears and almost as quickly disappears. Fortunately we are
spared the knowledge of what we are calmly breathing in and out in the
bus or the theatre. Because we have a limited range of eyesight and
are lacking in imagination we do not lynch the man sitting beside us
who spits on the floor.

The harmfulness of parasites largely depends on their numbers.
The adult stage of the herring-gull fluke which browses in the bird's
intestine does not seem to cause any inconvenience when only one or
two specimens are present. If the gull is unfortunate and catches a
very heavily infected fish similar to the specimen shown on Plate Vllb
and many thousands of flukes are liberated simultaneously in the
intestine, severe inflammatory conditions and even death may ensue.
It is true that single individuals of some parasites are dangerous. One
tick can provoke a mortal paralysis owing to its toxic saliva. On the
whole, however, such cases are rare. Broadly speaking, providing the
numbers of parasites are low the effects are slight. But accident or

THE EFFECT OF PARASITES ON THE HOST 33

circumstance may expose the host to a very high infection or permit
the uncontrollable multipHcation of the parasites within the body
which generally spells disaster. In order to soften Pharaoh's heart no
new parasites were created but the numbers of existing ones were
temporarily increased. When the dust turned to lice the importance of
this fact was no doubt appreciated by the Egyptians — " Then the
magicians said unto Pharaoh, This is the finger of God." It is this
problem of numbers upon which the host concentrates most of its
efforts and which it strives desperately to solve. Birds have developed
fidgeting, preening, dust-bathing, blinking and, in certain species,
"anting" (see p. 127) to such a fine art that ecto-parasites are generally
kept within reasonable bounds. Temporarily, at the end of the nesting
season, or if the host falls sick, their numbers may increase until they
assume menacing proportions, but this is unusual. The host has also
developed two main types of resistance to internal parasites. In some
cases, where small organisms are concerned, it imposes a sort of birth-
control on the invader and in other cases a curb on overcrowding,
like the housing act, and thus prohibits the development and establish-
ment of any further individuals of the same species in the same
individual host. This is a particularly effective method where helminths
are concerned. In fact, in many cases it is the early worm — and often
only the early worm — which gets the bird.

Both types of resistance can be demonstrated in the case of avian
malaria. During the ten days following infection the parasites are
found to accumulate very rapidly in the bird's blood. Then the host
falls ill and displays symptoms characteristic of the disease. During
this crisis the number of parasites in the peripheral blood stream in-
creases to a peak, but after about five days the bird recovers and the
parasites apparently disappear. However, a few are able to hang on in
the bone-marrow and the spleen where they continue to reproduce but
only in a very discreet manner. Then suddenly, for some reason which
remains obscure, the host's power of imposing birth-control on the
parasite seems to fail and there is a sudden increase in its numbers and
the sufferer has a so-called relapse. This feature is also characteristic of
malaria in man.

The reason for the sudden initial fall in the number of parasites is
principally due to their destruction by certain other blood cells of the
bird known as the phagocytes. A curious sort of armament race takes
place within the bird's veins and arteries. The phagocytes begin to

34 FLEAS, FLUKES AND CUCKOOS

increase in numbers soon after the malaria parasite is inoculated into
the bird. So do the parasites. Both increase more and more rapidly.
Sometimes the parasites occur in vast numbers — one infected corpuscle
to every ten healthy red blood cells is not uncommon. A desperate
running fight ensues — the phagocytes killing and ingesting the parasites
as quickly as they appear in the blood. Sometimes the parasites win and
their uncontrolled reproduction kills the host, but generally, in the
case of avian malaria, the phagocytes are victorious. The parasites are
destroyed — except, as we have pointed out, for a few isolated pockets of
resistance in the bone-marrow and the spleen. When the emergency is
over and the parasites have vanished from the outer peripheral stream
the number of phagocytes returns to normal. The standing army which
remains appears sufficient to cope with the ordinary situation. But
if the resistance of the host is lowered and the parasites again tempor-
arily get the upper hand, wholesale mobilisation of the phagocytes
occurs all over again. For the continuation of their life-cycle it is of
vital importance that Plasmodium should appear periodically in
large numbers near the surface of the host's body. Without these
occasional outbursts of reproductive activity they would never find
their way into the proboscis of the insect carrier. On the other hand it
is not in their interest to kill the host outright.

A great number of unknown factors may be involved in the so-
called lowered resistance of birds. The weather, particularly humidity
and low barometric pressure, the phases of the moon, the amount of
sugar present in the blood, exposure to ultra-violet rays, have all been
implicated and may be the direct or indirect cause of a relapse. In the
case of many parasites a bird's resistance varies with age. Tuberculosis
is pathological chiefly in old birds, whereas only young birds fall
victims to the attacks of certain worms.

In addition to phagocytosis the birds react to the presence of Plas-
modium by developing certain specific substances known as antibodies
in the blood serum and other body fluids. Their presence renders the
environment difficult or unsuitable for the parasite. This keeps the
numbers down after the initial reduction by the phagocytes — at any
rate any new infection by the same species is destroyed or unable to
develop. This phenomenon is known as partial immunity. Immunity
is the most widely studied of all the effects which parasites produce on
their host, for it has a wide practical application in medicine. In the
case of certain virus diseases such as small-pox in man and fowl-pox in

J. G. Bradbury
a. Common louse-fly, Ornithomya aviculmia, with fu'ly de\eloped wings ( x g-q)

^^kMJ^'

Arthur L. E. Barron J. G. Bradbury

b. Swallow louse-fly, Stenepteryx hiruudinis, c. Sheep keel, Melophagus ovinus, entirely

with non-functional wings ( x 5-1) de\oid of wings ( x 7)

Plate IX LOUSE-FLIES (HIPPOBOSCIDAE)

A. E. Bolting

Pronotal combs of, a. mammal Hca, Spibpsyllus cuniculi { x i8o), and
b, bird flea. Ceralophyllus galhnae ( x 212)

Plate .Y

THE EFFECT OF PARASITES ON THE HOST 35

birds, one attack confers a lifelong resistance or immunity against that
particular organism. Generally, in the case of the larger parasites
immunity is such that it prevents reinfection of the same species but
only while the infective organisms are still in the body of the bird. Thus
complete recovery — that is to say the death of the parasites — exposes it
to a fresh invasion. This state of affairs is so advantageous for the
worm or protozoan concerned that it might well be considered an
adaptation of the parasite rather than the host. In other words, the
host protects the parasite for life from intra-specific competition and
offers itself once again for spoliation by some other member of the race
if death removes the intruder. Simultaneously, of course, it also protects
itself from the crushing, possibly fatal, burden of over-population.

In the case of many endo-parasites of insects, superparasitism
frequently results in a battle between the larvae, only one surviving per
host. Thus intra-specific competition limits the number of parasites
and in this way achieves much the same results as the temporary im-
munity developed by the host itself. In the case of birds, if a heavy
initial infection occurs, and many larval worms are ingested simulta-
neously, intra-specific competition may also occur between the
developing adult worms.

This balance of power or mutual adjustment of parasite and host is
regarded as the hallmark of successful parasitism. Caullery considers
that in the case of such an infection the parasite and host together form
a functional balanced system which is placed in opposition to the ex-
ternal environment. In other words both parties make the best of a bad
job. The host's reactions — the result of selection — tend to reduce the
inconvenience to a minimum and the parasite has to live as unobtrusive-
ly as possible in a hostile environment. Together they must face the
dangers and hazards of the outside world.

In the case of larval flukes it is worth remembering that there can
be no gradual adaptation between host and parasite. Selection is
entirely one-sided. The parasite castrates the host, or in the case of
young snail hosts inhibits the growth of the gonads, and therefore the
more susceptible snails, and even those which survive infection the most
successfully, do not reproduce themselves and are eliminated from the
population. Consequently adaptation can only be on the side of the
parasite. In the case of larval flukes this situation is very obvious, but
it probably exists in many other cases of parasitism, when it is wrongly
assumed that adaptation is mutual.

FFC— D

36 FLEAS, FLUKES AND CUCKOOS

It is of course a well known fact that micro-parasites such as
bacteria and the viruses can, under certain circumstances, show an
increase or decrease in the pathological or poisonous effect they exert
on their host. The same phenomenon can be observed in various
parasitic Protozoa. For example, if the spirochaete which causes
relapsing fever in man is inoculated into mice, and passed rapidly
through a series of these animals, the organism loses its power to infect
man at the end of a few years. It is also noticeable how in many
epidemics, such as the influenza epidemic of 1948-49, the virus increases
in virulence as it passes from host to host. By the spring the disease was
far more serious than at the beginning of the winter. Certain try-
panosomes, such as the species which attack the big game of Africa,
exert no ill effects on those animals which are considered to be their
normal hosts, but prove virulent and fatal if they are passed to domestic
cattle. In other cases, such as pigeon-pox, the effect on unusual hosts
like the chicken is negligible in comparison with the effect on the normal
host. Again the introduction of other parasites may lower or raise the
virulence of an infection. Thus mild and chronic avian malaria in
canaries can be stimulated by the presence of spirochaetes, and
develop virulence and toxigenicity which soon kills the host. These
variations are often considered to be the result of selection acting upon
certain types already present in the infection or developed by muta-
tions. In bacteria they are frequently associated with morphological
changes. Such evolutionary trends can be observed in the case of
unicellular organisms owing to the numerous generations which follow
one another in rapid succession. The phenomenon is one of great
interest and practical importance but despite an immense amount of
research it is still not properly understood.

Turning now to brood parasites, such as the European cuckoo, the
attack on the host is relatively easy to observe. In the first place the
female destroys at least one egg of the host which she replaces by her
own. Subsequently, if the egg is accepted and incubated, the young
cuckoo, on hatching, destroys all the other eggs or nestlings which may
be present. Henceforth the entire efforts of the foster parents are
directed towards feeding and rearing the intruder chick. Frequently
birds desert their nests after a visit from the cuckoo, but even such cases
entail a considerable loss of time and effort on the part of the victim.
It must be remembered that a female cuckoo can, under favourable
conditions, lay over twenty eggs in different nests during a single

THE EFFECT OF PARASITES ON THE HOST 37

breeding season. One species of bird is generally parasitised in a
particular district and the cuckoo's attentions can result, over a period
of years, in a serious reduction in the numbers of the host. Some very
careful observations have been made on the reed-warbler in a circum-
scribed area in Germany. The first year in which counts were made
fourteen nests were present of which four contained cuckoos' eggs. Six
years later, in the same area, only eight were found and of these no less
than seven contained cuckoos' eggs. It seems quite possible that a
favoured host can be exterminated in certain districts by over-parasiti-
sation by the cuckoo.

It cannot be too strongly emphasised that the effect of all types of
parasites on the host is detrimental. If we find that a bird seems little,
if at all, inconvenienced by the presence of Protozoa or worms or lice,
or a cuckoo in the nest, we can nevertheless assume that it would be
better off without them. There are, for example, certain worms which
live in the oviduct of birds and are known to inhibit egg-laying. There
are others which are likewise located in the oviduct, yet apparently
produce no symptoms of any kind. Over a long period, however, they
may well reduce the total numbers of eggs laid. Small effects such as
lack of vitality, loss of voice, excessive blinking, or perverted habits
like dirt eating are extremely difficult to gauge. Nevertheless, it is
only a question of degree. Potentially all parasites are harmful.

Mussel, Mytilus eduLis, with a pearl

CHAPTER 5

THE EFFECT OF PARASITISM ON
THE PARASITE

Ruinous inheritance !

Gaius

A parasite's life is an impressive gamble. Indeed it is difficult to
envisage insecurity on such a scale. The chances of a grouse round-
worm finding a grouse are far less than the reader's chances of becoming
the parent of quads, or a cabinet minister.

Most free-living animals do not die of old age — they are killed and
eaten. The majority of parasites, on the other hand, die a lingering
death from hunger or exhaustion because they fail to find a host. As
Shipley pointed out, the eggs of the grouse roundworm lie scattered all
over Scotland, but millions and millions of their young, which hatch
out and wriggle up the sprigs of heather around them perish because
their particular plant is never eaten by a grouse. Similarly, vast
numbers of immature ticks cling hopefully to blades of grass, waiting
for the millionth chance which will bring an animal brushing through
the vegetation within reach of their waving forelegs.

Owing to the difficulty of finding a host — a difficulty which is
superimposed on the more familiar hazards of life — the mortality
among most parasites is enormous. A vast number of eggs or larvae
have to be produced in order that the species can survive at all. Con-
sequently a characteristic feature of most parasites is a relatively
enormous development of the reproductive organs, which frequently
come to dominate the body. Intestinal worms produce eggs by the
million and even brood-parasites like the cuckoo lay four or five
times as many eggs as their hosts. The difficulty of host-finding can
often be estimated by the number of eggs laid. Female ticks of the

EFFECT OF PARASITISM ON THE PARASITE 39

family Argasidae which live in the nests and burrows of their hosts lay
a few hundred eggs, whereas those of the family Ixodidae, which
generally have to depend on a chance meeting with their host in the
open, lay in thousands. There are also various peculiar asexual forms
of reproduction which help to increase the progeny of certain parasites.
Thus, each fertilised trematode egg, say of the herring-gull fluke
[Cryptocotyle lingua), by fragmenting inside the first intermediate host
(seep. 200), gives rise to several million larvae. Certain bird tapeworms
multiply by budding in the larval stage and by the production of
chains of individuals — strobilisation — in the adult stage. Parasitic
Protozoa, of which the malaria group is the best known example, have
the power of splitting up into several individuals once they have been
introduced into the blood stream of the bird.

The difficulty of finding a host is in itself a major issue but, added to
this, parasites experience great difficulty in finding a sexual partner.
Consider the position of two blood flukes which by the greatest possible
good fortune penetrate into the veins of the same duck. Consider the
further good fortune of these flukes if they happen to meet in their
progress through the interminable labyrinth of the host's blood vessels.
After two such coincidences they cannot possibly risk parting again.
It is, therefore, not surprising to find that devices for ensuring perma-
nent contact between such fortunate individuals are commonly met
with among parasites. The male of the duck blood-fluke {Bilharziella
palonica) has a flap of skin (the gynaecophorus canal) down the ventral
side of its body, in which it envelops the female. Henceforth the two
progress in a permanent embrace along the blood vessels of the duck
and the fertilisation of the eggs is assured. In the case of Collyriculum
faba, a fluke from the sparrow and other wild birds, and Balfouria
monogama, from the marabou stork, a male and female worm are snugly
enclosed together in a cyst, the formation of which they induce in the
tissues of the host. In the case of the sparrow fluke the cyst is situated
beneath the skin in the region of the cloaca and in the stork is an
invagination of the wafl of the stomach. The gape-worm {Syngamus
trachea), which is a famihar pest in the farmyard as well as a parasite of
many wild birds, lives joined together in pairs (Plate XXVIIb) in the
trachea and bronchial tubes of the host. Male and female are attached
permanently to one another by their sexual apertures.

In the case of some parasites the male is dwarfed and permanently
attached to the female. This is a curious phenomenon more frequent

40 FLEAS, FLUKES AND CUCKOOS

among animals which Hve in the sea than on land. There is one famous
example of a male roundworm which lives as a parasite inside the
vagina of the female. There is no doubt that this is a certain way of
ensuring that sperms are available when the eggs are ready for fertilisa-
tion, but like so many other devices to which parasites resort, it is
rather an exaggerated form of the more usual relationship between the
sexes. Among some ticks which also attack birds there are cases of
dwarf males parasitising the females to which they become permanently
attached (see tail-piece, Chapter 12). They pierce the skin of their
mates and gorge themselves on blood recently extracted from the body
of the host. Many internal parasites, however, have solved the problem
of fertilising their eggs in another way. Both male and female organs
are found in the same individual. Such two-sexed animals are known
as hermaphrodites and in many cases they are capable of self-ferti-
lisation and are completely independent. Marital worries are unknown
as far as tapeworms are concerned, for they can produce millions of
offspring in complete peace and solitude. Some hermaphrodites — for
instance quite a large proportion of trematodes — do, nevertheless,
copulate with another individual if the two should happen to meet in
the heaving darkness of the bird's intestines. There is no question of
waiting for the right sex — as copulation can take place between any
two mature individuals, a mutual penetration by the male organs
occurs and cross fertilisation results. Each partner then lays eggs.

Various parasites, for instance some ticks and nematodes, have
found yet another solution to the same problem. They resort to virgin
birth and in such cases their eggs develop without being fertilised.
Sometimes this form of procreation, which is known as parthenogenesis^
goes on for several generations, but when a male happens to be available
the female returns once again to the more usual form of reproduction.
In some species, however, only females have been found and it is believed
that the male sex has been dispensed with altogether.

In this way parasites are forced to adopt a dangerous procedure,
for asexual reproduction reduces the variability of the species con-
cerned. New combinations of mutations by sexual cross-fertilising
cannot occur, and such characters will remain isolated in each asexually
produced line or population. Huxley has stressed that the sexual
process confers a greater plasticity in evolution, and the parasite is
forced to sacrifice evolutionary potentialities by adopting partheno-
genesis, polyembryony and strobilisation in its efforts to reproduce

EFFECT OF PARASITISM ON THE PARASITE 4I

itself. It may have no alternative as a short term poHcy, but in the long
run such a procedure may prove fatal to the race.

Apart from the modifications connected with reproduction, there
are certain morphological features which recur persistently in para-
sites. Organs of locomotion are partially or totally lost. Intestinal
worms and leeches have no ambulatory processes. Parasitic insects
which live on the bodies of birds, such as feather hce, fleas and bugs
and certain flies, are wingless or have mere vestiges of wings which
for the purpose of flight are useless. On the other hand, they have
developed very varied and efficient organs of attachment, such as
hooks, suckers, anchor-like protuberances and prehensile lips — "for
their strength is to sit still." In the case of ticks, fleas and some
fly-larvae the mouth-parts, which are embedded in the host's flesh,
are armed with re-curved spines (see Plate XII). Leeches, on the
other hand, have cup-like suckers at both ends of the body, some
flukes chng grimly from the rear only, whereas lice hang on by
their claws. It is quite obvious that once a parasite has reached a
suitable host it must make every effort to remain with it. To be
sneezed out of the nasal cavity of a duck or blown out of an elephant's
trunk are very great dangers which leeches must guard against. Birds
with the "gapes" are racked by coughing — a sort of recurrent earth-
quake for the worms in their throats — and it is, therefore, scarcely
surprising that these nematodes live with their anterior ends embedded
in the mucous membrane of the bird's trachea. In a way, parasites are
caught between the devil and the deep sea, for often organs of loco-
motion would be extremely useful for finding their host, but a distinct
disadvantage once they have achieved this object. The parasitic fly
Carnus hemapterus, directly the bird host is found, quickly creeps
between the feathers, but first casts off its own wings. This is an un-
usual case. Generafly parasites lose their own organs of locomotion and
employ other transport animals (see p. i8 and tail-piece of Chapter 8)
in order to reach their host.

Many internal parasites absorb food through the surface of the body.
There is a tendency to lose their mouths and part, or all, of the digestive
organs. This modification is found in some Protozoa as well as in
worms and various other parasites. In ticks and leeches, which
frequently have to endure long fasts between their meals, portions of
the ahmentary canal are extended in the form of pouches and branches
in which the blood is stored and from which it can be absorbed slowly.

42 FLEAS, FLUKES AND CUCKOOS

Almost all the blood suckers — insects and worms, as well as leeches
and ticks — have developed a special sort of saliva which mixes with the
blood as it issues from the wounds they have inflicted and prevents it
clotting, both at its source and within the proboscis or gut of the
parasite. Many parasites also lack the sensory organs which normally
keep animals in touch with the external world. Eyes and ears would be
useless to a fluke in the liver of a bird, or to a feather mite in a curlew's
quill and, indeed, they possess neither. Instead they have developed
other senses or tropisms by which they are guided to small circumscribed
areas of the host's body or on long migrations through the tissues of the
host.

The difficulty of finding their host has imposed upon many parasites
a fantastically complicated life-cycle. Moreover most endo-parasites,
in order to reach their goal, must pass from a highly specialised but
stable environment into the strikingly different and fluctuating condi-
tions of the outside world. No man can leave an air-conditioned
hotel, say in Toronto, in mid-winter without putting on an overcoat,
but a parasite must face even more violent changes without any artificial
protection.

A few parasitic Protozoa pass from host to host during contact
between individuals — by licking, kissing, sexual intercourse or feeding
of young by the parents — but many form resistant cysts or spores which
pass into the outside world, where they are carried hither and thither
by the elements and possibly reach another host by the medium of
air or water or contaminated food. Some Protozoa are entirely
dependent on invertebrate vectors. The malarial parasites are perma-
nent prisoners in the circulatory system of their vertebrate host and
doomed to perish with it, unless they are rescued by a blood-sucking
insect. Only the sexual stage is passed in the mosquito and it seems
likely that the insect carrier has been secondarily interpolated in the
cycle. The opposite is probably true in the case of trypanosomes which
were primitively insect parasites.

The majority of worms have become involved with a complicated
series of intermediate hosts. Many bird flukes, for instance, have seven
stages : egg, free-swimming miracidium, sporocyst and redia within a
snail host, a free-swimming cercaria, an encapsuled metacercaria in a
second intermediate host (which can belong to almost any group of ani-
mals ranging from mammals and frogs to leeches and jelly-fish) and final-
ly the sexually mature individual in the bird (Fig. 4) . Sometimes an extra

EFFECT OF PARASITISM ON THE PARASITE 43

host is added or one cut out. The life-cycle of tapeworms is charac-
terised by the absence of free-swimming larvae but in many cases up to
four different intermediate hosts are used. Roundworms also frequently
depend on intermediate and transport hosts, and the filarias are taken
up from one host and put back on another one by blood-sucking insects.

Complicated life-cycles are unquestionably characteristic of internal
parasites. On the other hand extremely simple life-cycles are met with
among external parasites, particularly those like feather lice, mites, and
the sheep ked, which pass generation after generation on the same
individual animal. Parasites, it is true, develop many features in
common but free-living organisms become adapted to a specialised
environment in the same way, and we find for instance that cave-
dwelling animals all over the world are often characterised by blind-
ness and pallor. Parasitism merely provides a particular habitat and
mode of life which calls forth certain equally distinctive adaptations.

Some parasites are able to live on a wide range of hosts belonging
to different orders or even classes of animals, but it is more usual for a
parasite species to be confined to a relatively small group of hosts.
These may embrace a whole order such as the ducks, geese and swans
(Anseriformes) or two or three related species like the swallow and house-
martin, or even a single species or even subspecies of bird Parasites
which are confined to one particular host, or to a group of related
hosts, are said to be host specific.

Host specificity is the result of the parasite adapting itself to life in a
certain environment, and if the adaptation is very close it is unlikely
that it will be able to survive on, or in, any other host. Many free-
living animals have become adapted to particular environments or highly
specialised diets, and are therefore unable to live elsewhere. The
crested tit in Scotland is restricted to areas where there are old rotten
pine stumps in which it nests. The marsh fritillary butterfly {Euphydryas
aurinia) in Britain is confined to an environment where the devil's-bit
scabious is found — the only plant upon which the female will lay her
eggs, although the larva will feed on honeysuckle, snowberry and
certain other leaves. The koala bear can only survive on a diet of fresh
eucalyptus shoots and is therefore restricted to places where the plant
grows. Such examples could be multiplied indefinitely. It may
originally be a single attribute which links a parasite to one particular
animal but once the association has begun all the characteristics of the
host, morphological and physiological, as well as biological, play their

44 FLEAS, FLUKES AND CUCKOOS

part in guiding the parasite along certain well defined lines of develop-
ment. The permanent ecto-parasite becomes adapted to the external
covering of the host — the feathers or hair and the skin texture. Such
characters affect the mouth-parts of the parasite, its integument, and
claws. Certain feather lice in which adaptation has become very close
cannot lay their eggs on feathers of a different structure from that of
their normal hosts. In other cases ovulation and hatching can only take
place within very narrow ranges of temperature. The fertility of the
eggs may also depend on whether the parasite has fed on the right host.
Many ecto-parasites seem to be closely adapted to the chemical com-
position of the blood and feathers of their host. In a carefully controlled
experiment Wilson has shown that one of the chicken lice would feed
on feathers of an American heron, but the nymphs did not complete
their moults and the adults died within three to sixteen days. Some
bloodsuckers placed on an abnormal host will often refuse to feed,
others attempt to do so without enthusiasm or success, while others
again will imbibe the strange blood but die shortly afterwards. As
Lucretius remarked, " What is food to one man may be fierce poison
to others."

Most lice are strongly host-specific, but a notable exception is the
species from pig and man. The human louse will feed and breed on
swine, and the pig louse is equally at home on man. There is an obvious
resemblance between the near naked skin of the domesticated pig and
man, and again, the chemical composition of their blood must have a
lot in common — at any rate neither proves lethal to the lice in question.
There are other parasites which normally feed on these two hosts :
the human flea [Pulex irritans) and the jigger {Tunga penetrans)', a tick
[Ornithodoros moubata); certain of the floor maggots {Aucheromyia) , a
nematode worm {Ascaris lumbricoides) and the influenza virus.

In some cases, when a parasite appears to live normally on a strange
host some part of the biological cycle is nevertheless disturbed. The
human louse breeding on the pig produces an abnormally high
proportion of females — a factor which could lead ultimately to the
extinction of the race.

Where endo-parasites are concerned the chemical composition of
the various body fluids is probably of much importance, and also the
composition of the gut contents, and the physical structure of all
the internal surfaces which the parasite pierces or clings to during the
course of its life-cycle. The rapidity with which food passes through an

EFFECT OF PARASITISM ON THE PARASITE 45

animars body, for instance, can determine which cysts have time to
hatch before they are ehminated.

In all types of parasites there is a close adaptation to the habits of
the host. Sand-martins dig long burrows in sand quarries, place their
nests in the excavations, and return to them year after year, and thus
expose many of their ecto-parasites to peculiar and unusual conditions,
combined with severe isolation — which is also a factor conducive to
speciation. It is therefore significant but not surprising to find that
sand-martins have at least two fleas, a tick, mite, fly and beetle, all of
which are host-specific.

The feeding habits of certain animals expose them to infection by
worms which use their prey as transport hosts. This frequently results
in a sort of pseudo-host-specificity. Thus certain flukes which are
found in nature in a few species offish-eating gulls will develop success-
fully in a wide range of hosts in the laboratory, including dogs and
rats. The distribution of adult flukes is chiefly governed by the feeding
habits of the final host and has been called ethological specificity by
Baer. He contrasts this with the type demonstrated by the tapeworms
of birds, which he designates as phylogenetic specificity. In their case
specificity is strongly developed, a fact which he suggests is due to their
very ancient association with their hosts.

It is of great interest that, unlike the adults, the first larval stages of
trematodes are markedly host-specific. This fact has led many people
to suggest that flukes were primitively parasites of molluscs and that
the adult stage in vertebrates is a relatively recent development. This
might account for their lack of specificity in the adult stage. Tape-
worms on the other hand are rarely host-specific in their larval
stages.

In the case of permanent obligate parasites, such as feather lice and
mites, which pass several generations upon the same bird, there are few
disadvantages and many advantages in host specificity. They may be
compared to the fauna of oceanic islands, which have few oppor-
tunities for extending their range to other lands and relatively little
competition from invading species, and can consequently adapt
themselves more and more closely to the specialised conditions of
their own particular habitat. This enhances further the prospects of
the individual, enabling it to live and breed more efficiently and to
achieve a relatively harmonious personal relationship with the host,
without endangering the survival of the species.

46 FLEAS, FLUKES AND CUCKOOS

The fauna of an oceanic island is also subjected to intense isolation
over long periods of time, circumstances which, as we have already
mentioned, are known to favour the formation of distinct species. The
same factors operate in the case of permanent bird parasites. The
obligatory restriction of the feather louse population to a particular
bird host enables it to form distinct species and to develop characters
which make it impossible for it to live on other species of birds; the
more distinct the species the greater the ensuing isolation, consequently
the process is cumulative and host-specificity becomes both its own
cause and effect.

In the case of temporary parasites which only visit the host at
intervals to partake of a blood meal, host-specificity is fraught with
great danger, for the chances of finding one species of host after long
periods of separation are often remote. On the whole, parasites like
ticks, mosquitoes and leeches are not host-specific, although with a
combination of special circumstances like those we have mentioned for
the sand-martin strict specificity can develop.

In the present state of our knowledge, however, it is often impossible
to recognise, let alone explain, the various adaptations which limit
parasites to single hosts. The common hen flea {Ceratophyllus gallinae)
for example is an insect with remarkably catholic tastes. It has been
found (see p. 1 1 1) on over a hundred different species of bird host. A
closely related species (C rossittensis) , almost indistinguishable mor-
phologically is, on the other hand, closely confined to the carrion-crow.
Such cases are not understood and for the time being must remain a
mystery.

A strictly host-specific parasite like the crow flea is closely adapted
to a dependent condition — a situation which is fraught with great
danger. Even in the case of free-living animals restriction to a single
source of food can lead to disaster. If some unforeseen event, such as
a sudden change in climate or the spread of some rare disease, destroys
the hitherto plentiful food supply the species of animal in question
cannot survive. In recent years large numbers of brent geese perished
during the sudden worldwide famine of eel grass. As a few individual
birds still retained the possibility of changing their feeding habits the
species was enabled to weather the crisis. One of the great ironies of
life is that the most spectacular and successful specialisations of to-day
frequently spell doom and destruction for to-morrow.

CHAPTER 6

THE ORIGINS OF PARASITISM AND THE
EVOLUTION OF PARASITES

How Mutability in them doth play
Her cruel sports . . .

Edmund Spenser

I HERE ARE no parasitic starfish or lampshells but in all the other
large groups we find animals which have abandoned a firee life in
favour of parasitism. Zoologists have Httle, if any doubt that all para-
sites have evolved from free-living animals. Many such organisms are,
of course, at different stages of evolution, some being much farther
removed structurally from their ancestral stock than others and
consequently resembling them less and less. Before the larval stages
of these animals were known their origins in many cases remained
obscure. Now that the life-cycles have been worked out their past has
been revealed. Thus, for example, the dog whelk has a free-swimming
larva known as a veliger and so has the worm-like, shell-less, footless,
colourless, toothless gastropod mollusc {Entoconcha mirabilis) which lives
as an internal parasite of sea cucumbers (Holothurians) . Fish-hce, too,
some of which as adults resemble Httle bags of blood fixed to the gills ol
fish, have an active swimming larva very similar to the larva of the
free-living copepods, which swarm in the sea. An endo-parasite
[Sacculina] which resembles a mass of roots ramifying through the inter-
nal organs of crabs, has a free-swimming larva which instantly reveals
its true nature and places it among the barnacles (Cirripedia).

These are extreme cases. Most parasites are not modified beyond
recognition. As we have seen in the foregoing chapter certain struc-
tural alterations are associated with the parasitic mode of life, but we
can still find in most of them a well-marked resemblance to their free-
living relatives. There are, however, no free-living tapeworms or

FLEAS, FLUKES AND CUCKOOS

flukes in existence but although their origins are obscure the larvae
reveal traces of an independent past. In many groups of animals
parasitism has arisen anew several times over, a fact which is confusing
and irritating for zoologists as it seriously interferes with their desire for
orderly pigeon-holing.

Parasitism can develop gradually or suddenly. It can be the out-
come of a long series of complicated interactions or the result of isolated
accidents which occurred a million years ago or only this morning. A
long established and widespread habit, such as the wanderlust shown
by mites, together with their inclination to creep into cracks and
crevices, may be the starting point. On the other hand some unusual
occurrence such as the accidental introduction of a number of uni-
cellular organisms into a bird's inside, with its food or water, or with
the air it breathes, may provide exactly the right conditions and
circumstances required to induce them to begin the parasitic mode of life.

Many animals are saprophagous, that is to say they feed on dead and
decaying matter, such as dung or putrefying corpses. It is a short step
from a dead nestling to a decomposing flesh wound on a living bird, and
the fly-larvae, which occasionally try the latter as an alternative meal,
are following one of the well-trodden paths to parasitism.

Many of the arthropod parasites of birds, such as bugs, mosquitoes,
and ticks, were originally suckers of plant juices. As the geological
record proves, these groups evolved before birds and mammals and,
no doubt, in the past were essentially vegetarians. It is a relatively
easy matter for them to pierce the skin of an animal either accidentally,
in error, or deliberately if no other food is available, and to extract its
body fluids. These accidental and casual drinks of blood which no
doubt originally took the form of an occasional meal might easily
become a habit, and then a necessity. Blood appears to be a somewhat
dangerous beverage, for like alcohol, it can convey certain immediate
advantages, yet carries with it the dreaded seeds of dependence. In the
case of careless blood drinkers the sins of the parents may be visited
upon the children in dramatic fashion — even unto the millionth
generation or more.

Competition for living space is very keen in nature. Even such un-
attractive milieus as vinegar, gall and crude petroleum have been
successfully populated by certain species of worms and fly-larvae.
Sometimes an ecto-parasite finds competition too intense on the surface
of the host's body and creeps into a convenient orifice, a step which

ORIGINS OF parasitism: evolution of parasites 49

can eventually result in a change to an endo-parasitic mode of life. It
is not, of course, suggested that all internal parasites have passed
through an ecto-parasitic stage.

The females of many animals are predisposed to take this route, for
they frequently seek sheltered nooks and crannies in which to breed.
We find that the females of the roe-deer flea {Dorcadia dorcadia), for
example, are fixed permanently inside the nostrils of their host, but the
males are free and wander about over the whole body.

One species of black-fly (Simuliidae), of which the males are not
parasitic at all, mates in the ears of its host — for where the female
leads the male follows and in due course both sexes may take to an
endo-parasitic life.

Numbers of temporary insect parasites are only parasitic in the
female sex — the males feeding romantically on dew and nectar. In
many cases the development of fertile eggs has become dependent on a
blood meal and so tied the species to a vertebrate host.

There are multiple ways in which parasitism can arise and in fact
there is only one vital element in the genesis of a parasitic relationship
and that is opportunity. Flies are continually, although unwillingly,
brought into contact with spiders and it comes as no surprise to find
a group of flies (Cyrtidae), which in the larval stage parasitises spiders.
Ducks eat leeches with extreme relish and there is one case on record
when some of these birds arrived overnight at a leech farm and by
breakfast time had devoured the entire stock of 20,000 leeches. Never-
theless we find that at least one species of leech parasitises ducks. There
is an even more curious situation existing between certain birds and
mosquitoes. Swallows, for example, devour them by day and by night
are devoured by the insects.

The most favourable condition, therefore, for the dawn and develop-
ment of dependence is a social environment and it is in crowded
communities, whether of birds or ants or men, that one finds parasitic
relationships developed most consistently. Here the scene is set, the
dangerous opportunity is ever present, and it is merely a question of
time before one of the organisms concerned exploits the situation. It
may thereby obtain some advantage, however transitory, which starts
it upon a course of irreversible specialisation — the risky road to
dependence.

A commensal relationship is potentially even more dangerous than
a merely social tie, for by nature it is more intimate. The closer the

50 FLEAS, FLUKES AND CUCKOOS

association, the more easily is the balance upset. One partner can
then suddenly take a mean advantage of the other. Thus we have
already seen that certain debris feeding fly-larvae which find shelter in
birds' nests will sometimes return their hospitality by surreptitiously
eating the fledgelings alive. Some of the predatory mites, which live
permanently on birds and hunt other small arthropods in the forests of
feather and down, have abandoned the chase and turned parasitic
themselves. They have lost their powerful jaws and now chew the pith
of feathers or the various layers of the bird's integument. Although
commensals obviously expose themselves to treachery of this sort, it
would be entirely wrong to imagine that commensalism is an inevitable
step in the development of the parasitic habit. It merely represents one
of a number of ways in which parasitism can arise.

In the cases we have cited the prey is a small animal, which has
occasionally been able to turn the tables on the predator by becoming a
parasite. The more usual course of events is for the predator itself to
find the prey too large to kill but nevertheless it can feed upon it and be-
come permanently attached to it. This is undoubtedly one of the
commonest ways in which the parasitic habit has originated. Some
leeches, which have not developed a specialised taste for one particular
food, will kill any small animal they come across in their wanderings
in ponds and streams. They attach themselves to their unfortunate vic-
tims and suck them dry. If, however, a leech finds an elephant taking
a casual bathe in the river and can creep into its anus, the days of pre-
carious wanderings are over. However successfully and however long a
leech maintains this position it will certainly never suck the elephant
dry. Large size is fundamentally a bar to the parasitic habit. An
elephant's trunk, like the leech's sucker, may pre-adapt it to ecto-
parasitism, but it is clearly impossible for any large mammal to secure
a life of ease and plenty in such a manner.

The rove beetles (Staphylinidae) have developed a wide range of
habits. The majority are saprophagous and swarm where there is dead
and decaying organic matter such as dung and corpses, but many are
predacious, both as adults and larvae. A large number of these beetles
are found exclusively in the homes of other animals. We can guess that
they were first attracted to this habitat by the concentration of animal
life or animal excrement and later became adapted to, and possibly
largely dependent on, the higher temperature characteristic of nests.
In the case of the species which favour the homes of birds and mammals

c d

Photographs by Arthur L. E. Barron

The shearwater flea, a, Ornithopsylla laetitiae (male, x 17), is related to the rabbit flea,
b, Spilopsyllus cuniculi (male, x' 22), whereas the hen flea, c, Ceratophyllus gallmae
(male, /' 19), is probably derived from a rodent flea similar to d, Ceratophyllus anisus

(male, x 20)

Plate XI

J. G. Bradbury
a. Blow-fly, Calliphora sp. ( x 24)

Arthur L. E. Barron

b. Hen slick-tight flea, Echidnophaga
gallinaceus (female, x 136)

Martin Duncan Arthur L. E. Barron

€. House-gndLt, Culex pipiens, {[emale, x 57) d. ^hecp lick, Ixodes ricinus (female, x loi)

MOUTHPARTS SHOWING ADAPTATIONS TO SPECIALISED
METHODS OF FEEDING
Plate XII

ORIGINS OF parasitism: evolution of parasites 51

they have retained the more primitive predacious habits and are gain-
fully employed, as far as the host is concerned, killing and eating their
flea parasites. In the intensely social environment of a termitary or
ant hill the behaviour of the staphylinid beetles has radiated out along
several different lines. Firstly, the predatory habit has developed into
straightforward parasitism and the larvae of some species are parasitic
upon the nidicolous pupae of certain flies. Secondly, there are species
which are commensals of the ants. They live as tolerated guests and,
for example, accompany the foraging expeditions of the legionary
ants, picking up some of the food captured on the way. They have
come to resemble their hosts to a remarkable degree. Thirdly, there
are scavengers and corpse eaters. Towards this category the ants show
a certain degree of hostility — with good reason, because in the case of
diseased and disabled workers, the beetles sometimes reduce them
prematurely to the status of a corpse. Fourthly, there are the symbiotics
which, like those from birds' nests, prey on certain enemies of the ants,
such as parasitic mites and the larvae of certain flies. Finally, we have
the true guests (symphiles) which are housed, fed and even reared by
the ants and, in return for their hospitality and solicitude, eat their
eggs and young. To encourage their ministrations the beetles exude a
glandular liquid which the ants find madly attractive and lick up with
intense eagerness. It is not known if the liquid exuded by the beetles
confers any benefit on the ants. It appears more probable that they are
merely sacrificing their brood in order to indulge an irresistible craving
for the exudation — a situation which the beetles have learned to exploit.
Such curious behaviour is also found in human communities where men
will sacrifice their own health and the welfare of their families in order to
indulge in drugs and drink.

Thus it will be seen that, once established in a communal environ-
ment, the rove beetles have exploited the situation in a variety of ways.
They have launched out into different kinds and different degrees of
commensalism, symbiosis and parasitism.

There are certain features (see p. 38), both morphological and
biological, which appear to be characteristic of parasites. These
attributes are useful and adapt them to the parasitic mode of life, in the
same way that the streamlined shape of whales and sharks adapts them
to a wandering life in the sea. How these modifications have come about
is the subject of much discussion. Parasites themselves are very varied
organisms, pertaining to widely separated groups of animals, and it is

FFC— E

52 FLEAS, FLUKES AND CUCKOOS

highly improbable that in their case every kind of evolutionary change
is brought about in the same way. Mites and feather lice, for example,
pass generation after generation on the same individual host and,
where they are concerned, one can expect to find evolution working in
much the same way as it does on the fauna of a small oceanic island.
Competition between members of the same species of lice and the same
species of mites, both for food and accommodation, must be intense.
On the other hand, certain intestinal worms battle in solitude with the
host, the elements and space — for them intra-specific competition plays
a minor role.

Some zoologists believe that natural selection, acting upon chance
mutations, gradually alters parasites and adapts them to their special
mode of life. In experimental breeding of the small fruit fly [Drosophild)
several mutations are known to occur producing wingless flies, or flies
with sickle-shaped or greatly reduced wings, which are reminiscent of
some of the types found in nature in the various species of parasitic
louse-fly. Such mutations may be advantageous for a parasite and
consequently on certain hosts the wingless type would stand a better
chance of surviving and reproducing itself. It is also thought possible
that certain features of a parasite's environment, for example, the ecto-
parasite's contact with the constant heat of the bird's body, or the fact
that many worms and Protozoa are permanently immersed in their
food, act in such a way that some types of mutations are favoured or
even induced; natural selection would subsequently determine their
survival value. This theory may apply especially where minor adapta-
tions are concerned — such as the similar comb-like structures found on
the bodies of very dissimilar insect ecto-parasites like certain flies, fleas,
beetles, lice and bugs.

On the other hand some biologists argue that in order to start on
this peculiar form of existence an animal must be pre-adapted to para-
sitism. Baer surmises that the louse-flies possessed a tendency to
regression of the wings, blood-sucking habits and viviparity which
destined the group to a parasitic life. In support of this theory it must be
pointed out that the features which are characteristic of parasites are
by no means peculiar to them. Thus, some tapeworms will lay one
hundred and fifty million eggs a year, whereas the estimated annual
output of a free-living starfish is upwards of two hundred million.
Animals such as the limpet and the common goby have efficient
suckers with which they cling to wave-swept rocks. Some female deep-sea

ORIGINS OF parasitism: evolution of parasites 53

fish have dwarf males which hve on them as parasites and many
molluscs are hermaphrodites. Snakes and earthworms have lost their
legs or ambulatory processes and certain jelly-fish are capable of
absorbing nourishment through their skins. In these cases the factors
which determine a vast output of eggs, the development of suckers, the
loss of organs of locomotion and so forth, obviously have nothing to do
with a parasitic environment. It is easy to see that any animal might
already possess one or several of these specialisations before it took to the
parasitic mode of life. Furthermore, the difficulty experienced, say, in
reaching a new host is obviously so great that it is hard to conceive how
such an animal could become established as a parasite unless it already
possessed immense powers of reproduction. The theory of pre-adapta-
tion is, therefore, undoubtedly attractive in the case of species which are
introduced suddenly and violently into an entirely new environment.

It is as well to remember that if individuals vary at all pre-adapta-
tion must exist. Some of our friends seem to enjoy heat waves, while
others become inactive and sit around sighing and mopping their
brows. It is permissible to claim that the former are pre-adapted to
a hotter climate. Professor J. B. S. Haldane once demonstrated at a
Royal Society Conversazione that he is immune to the bite of bed bugs.
So was his father. The Haldane family are therefore pre-adapted to
survive a bug-borne epidemic, should one occur. To say that plants and
animals may be pre-adapted is really only another way of saying they
are not all alike, for every variation is potentially both adaptive and
pre-adaptive. On the other hand, as Bodenheimer has pointed out, in
one sense no real adaptation to a new environment ever takes place.
No matter how different life may be, say, in the sea, or in the gall-
bladder of a bird, an animal's response cannot surpass the hereditary
base of reactions. Theoretically evolutionary possibilities are endless,
but certain lines are mutually exclusive, and once an animal has
started along one of these evolutionary paths, others are automatically
barred. The more highly specialised an animal becomes the less are
its chances of being able to break away, and certain lines are thus self-
directing and self-restricting. Therefore, although Sacculina develops
root-like extensions of the body which ramify throughout the host's
tissues, it cannot turn into a plant — although such a transformation
might have definite advantages.

There are also some very interesting examples of direct modifica-
tions which have been produced merely by a change of host. For

54 FLEAS, FLUKES AND CUCKOOS

instance, the sexual form of certain roundworms develops directly from
the egg in sheep, but in rabbits the same worm produces an asexual
generation. In a few abnormal hosts worms are dwarfed, or only one
sex — the male — -may achieve development. Again, variable strains of
trypanosomes are known which are dependent upon and produced as a
response to the environment in a particular vertebrate host.

Whatever theory is favoured, from the point of view of the biologist,
parasites remain a particularly interesting and fruitful study. For,
although there are no fossils with which to compare parasites, free-
living forms from which they must have been derived are often available
and the two can be examined alive side by side. The zoologist can look
at an active free-swimming copepod dashing about in the water with
its antennules twitching and its swimmerets beating, and he can also
examine the parasitic fish louse, attached like a small sack of blood and
eggs to the host — and stare in amazement at the results of evolution.

It is probable that parasitic animals exceed non-parasitic forms,
both in the number of existing species and in the number of actual
individuals. For example, from man — not counting bacteria and fungi
— over five hundred different species of parasites are recorded. This
mode of life consequently appears, at first sight, to be highly profitable.
However, the evolution and progressive transformation in the direction
of successful parasitism clearly reduces and circumscribes the possibility
of future readjustments. Huxley has defined biological progress in its
broadest sense as "control over the environment and independence
from it." The evolutionary trend of parasites is in the opposite direc-
tion— towards dependence.

We have already called attention to the fact (p. 7) that many
animals can be parasitic for some period of their lives and yet show no
trace of this particular mode of existence, either in form or function,
during other stages of their life-cycle. There are also those cases in
which one sex is parasitic and the other is not, and the free sex displays
no modifications which can be attributed to the strikingly different
way of life chosen by its mate. Furthermore, whether we are dealing
with a coot or a cuckoo, a butterfly or a bed-bug, an earthworm or a
lungworm, we find that the eggs and sperm of both free-living and
parasitic animals are remarkably alike.

It would certainly appear that a parasitic existence during the
larval stages of an animal's life-cycle is neither so harmful nor so
irrevocable as in the adult stages. Many entomologists believe that the

ORIGINS OF parasitism: evolution of parasites 55

Hymenoptera, including the most highly developed of all insects, the
social bees and ants, are descended from ancestors which were parasitic
in their larval stages. Keilin has put forward strong evidence to show
that the Cyclorrhapha flies, which include the house-flies, bluebottles and
their allies, are likewise descended from ancestors all of which had
parasitic larvae, although at the present time only a small proportion
have retained this habit.

It is perhaps obvious that the benefits bestowed on an organism by
the parasitic mode of life would be most marked in its immature stages.
During the period of maximum growth it is sheltered from the rigours
of the outside world and protected from violent changes in the environ-
ment. It is also provided with an abundant and constant food supply.
Moreover, its close relationship with the host is for a limited period
only, which does not involve the permanent sacrifice of independence,
nor the loss of those sense organs which constitute its link with life in
the outside world.

The French zoologist, Giard, gave the name of "placental parasite"
to the mammalian foetus. Many biologists strongly object to the term
"parasite" used in this sense and consider that it cannot be employed to
indicate a relationship between individuals of the same species. Never-
theless, the fact remains that during foetal life the mammalian young
obtains food, water and oxygen from the body of the mother and
through the organ of attachment — the placenta — excretes the waste
products of metabolism. Various reactions, not always beneficial, set
up by the presence of the foetus, are singularly reminiscent of those
brought about by an alien organism feeding at the expense of the
host. In fact, placental parasitism represents the supremely successful
example of this mode of life. It seems possible that a fundamental
distinction can be drawn between the parasitic adult and the parasitic
young, the full significance of which has not hitherto been fully appreci-
ated. In the former, parasitism appears to lead to dependence and a
loss of evolutionary potential, whereas in the immature stages, it may,
on the contrary, prove to be a successful and progressive step.

PART TWO

Bird Fleas and Feather Lice

INTRODUCTION

Sir, there is no settling the point of precedency
between a louse and a flea.

Dr. Johnson

BIRD FLEAS and feather lice do not sing. Nor do they fly about
flashing brilliantly coloured wings in the sunshine. It is scarcely
surprising that in Britain bird and butterfly enthusiasts number
thousands, but the collectors of fleas and lice can be counted on the
fingers of one hand.

The Mallophaga and Aphaniptera are small, drab insects of in-
significant appearance and without obvious aesthetic appeal. In the
mind of ordinary men and women they have loathsome associations of
dirt, disease and furtive scratching. Moreover, they are too small to
study with the naked eye and the finer structures on which their classi-
fications are based have to be examined with the aid of a microscope.
From the scientific aspect however, they are of great interest, not only
as carriers of deadly disease but as insects closely adapted to the
parasitic mode of life.

Both bird fleas and feather lice prey upon avian hosts, and their
mode of life has imposed upon them certain well known features
associated with parasitism. Thus both are wingless, both have failing
or poorly developed eyesight, and both have claws adapted to clinging.
In addition they have developed a very resistant integument, and can
consequently survive a nip from the host that would squash or fatally
injure many insects of similar size. The Ceratophyllid bird fleas and a
certain number of species of Mallophaga also share a rather curious

INTRODUCTION ! PART TWO 57

adaptation. The males have antennae especially modified for grasping
the female during copulation.

Despite these features which they have in common, the two orders
present a profound contrast.

First of all the feather louse undergoes no metamorphosis. When it
hatches from the egg, a feat it accomplishes by pushing up the cap which
opens like a lid, the nymph or young louse which emerges is more or
less a miniature edition of the adult — minus the sexual organs.

It reaches maturity by a series of three moults, that is to say it
periodically casts off its integument for which it has grown too big.
Each time it changes its skin in this manner it becomes a httle more like
the perfect insect. Its whole life-history from egg onwards is passed
upon the host, and from the day it hatches it can chew feathers. The
feather louse's world is the hot, fidgeting body of the bird, with which
its fate is indissolubly linked. The reproduction of the host means a
future for the louse and the death of the host spells its inevitable doom.

Fleas on the otherhand, have a complete metamorphosis (Plate
XVIII). The larva, which develops inside the egg, hatches by ripping up
the egg-shell with a special spine situated on the front of the head. The
sort of legless caterpillar which emerges does not remotely resemble a
flea, and at this stage chews its food rather Hke a feather louse. After a
series of moults it changes into a pupa, or resting stage, from which, in
due course, the perfect insect emerges. Unlike the larval stages of the
feather louse, those of the flea are free and are generally passed in the
host's nest.

In many cases fleas themselves only spend a limited amount of
time on the body of the host, and should the bird die they can survive
for days, weeks, or even months, hiding in the nest or some appropriate
crack or crevice. They can also live for a long period after emerging
without food, but ultimately they are compelled to partake of a blood
meal or perish without reproducing themselves.

Structurally the adult insect also presents a considerable contrast.
Fleas are flattened from side to side, essentiafly an adaptation to
life in fur. Only a very fat man who has once been thin can apprec-
iate the advantage of not having to turn sideways to get through a
gap, especiaUy if he happens to be in a hurry. On the host, fleas are
nearly always in a hurry.

Feather lice on the other hand are flattened from above downwards.
Their life depends on being able to cling closely to the feathers, or,

58 FLEAS, FLUKES AND CUCKOOS

in Other words, to protrude as little as possible above the surface of the
host.

Fleas are, generally speaking, much more active insects than lice.
They have more need to be. The feather lice can run, but they generally
confine themselves to sudden short rushes which enable them to move
quickly out of sight if they are momentarily uncovered by the bird's
preening.

Species restricted to the head or neck, out of reach of the host's
beak, can sacrifice speed and become more closely adapted to the
feathers. Fleas, except for one or two rare exceptions such as the
stick-tight flea of poultry (see p. 62), not only have to move rapidly
on the host, but they need to jump on and off at very short notice.
Hence they are provided with long powerful legs, whereas those of the
feather lice are short and weak.

It is perhaps unnecessary to stress the fact that the feather lice bite
and chew their food, while the fleas suck it up in liquid form through
tube-like mouth-parts (Plate XII). Expressed differently, the latter
cannot eat, they can only drink.

It is when we come to regard these two groups of insects as a whole
that we realise how great the contrast is between the two.

Ornithologists calculate that there are approximately 8,500 species
of birds in the world to-day. Louse experts estimate that there are more
than three times as many feather lice, making a total of approximately
25,500 species. Of bird fleas about 60 are known and named. Possibly
the total is somewhere around a hundred.

The feather lice show great diversity in form and structure, whereas
the fleas, at least to the naked eye, present a very homogeneous
appearance. Again, each order of birds has its own characteristic
feather lice — -just as it has its own Cyclophyllid tapeworms — whereas
the bird fleas show no such restriction to a group of hosts. Moreover,
many species of feather lice are host-specific, that is, confined to a single
species of bird, whereas most of the fleas are not. Finally many feather
lice have specialised habitats upon the bird's body — some are confined
to the head, others to the wing feathers, others again live inside the
quills. Except for the two or three species in which the females are
sedentary and therefore obliged to congregate on the head (see p. 76),
fleas have no special location on the host's body.

Thus an immense gap divides these two orders. The feather lice,
one can deduce, are a very ancient group. They are also a highly

introduction: part two 59

successful group on birds, less so on mammals. Fleas, on the other
hand, are not successful as bird parasites. They primarily prey upon
mammals and only a few have succeeded in changing over to bird
hosts. Up to date no one can say it has been an advantageous step and
so far the order has failed to expand on birds.

Perhaps the greatest interest of the feather lice arises from the fact
that they have, through the ages, been saved many hardships and
violent changes of environment which the birds themselves have ex-
perienced. For this reason and also perhaps because their evolution
proceeds, fundamentally, at a slower tempo, they have evolved and
differentiated less rapidly. Thus the feather lice have not diverged so
widely from the parent stock and by their resemblance to one another
they can reveal the original but now hidden relationship of the birds
themselves. The parasites' environment has remained comparatively
stable. For example, the temperature of a bird's body is relatively
constant whether it is living in the Alps or in the Sahara. The composi-
tion of the feathers and blood on which the parasites feed is also
relatively stable, whether the bird is living on a diet of wire-worms,
berries, fish, green leaves, carrion or grain. The hosts themselves have
had to contend with great geological and climatic changes, and also
new habitats into which they are forced by competition, which in turn
have involved changes in their mode of life and diet. In such circum-
stances the birds respond by physiological and morphological changes
which often conceal their true descent.

There are many groups of birds which are a puzzle to the systemat-
ists and which are difficult to place in any scheme of classification.
What is the rightful place of the flamingoes— with the ducks or with
the storks ? Are the humming-birds related to the swifts or passerine
birds ? Are woodpeckers correctly placed in a separate order ? In
Chapter 8 we shall consider the evidence provided by the feather Hce
which infest birds, and see what light these throw on the classification
of their hosts.

Strong criticism is sometimes levelled at parasitologists regarding
the evidence of host relationship drawn from a study of parasites. It
is argued that a mistake can as well be made regarding the systematic
position, say of feather louse or a tapeworm, as of the bird itself. With
this we entirely agree, and we would not therefore accept as strong
evidence of relationship, the sharing of say one genus of parasites by two
hosts. However, when a bird of doubtful position harbours three

FLEAS, FLUKES AND CUCKOOS

genera of feather lice common to some possibly related group of birds,
wc consider the evidence of relationship strong — for three major
errors in the interpretation of louse morphology would be improbable.
In all cases, however, the evidence presented by both host and parasite
has to be carefully examined and sifted because of other factors (see
p. 141) which may be involved. As yet there is little co-operation
between one type of specialist and another. There is a natural
tendency for the ornithologist to place more reliance on the work of his
fellow bird specialists, which at least he can appraise, than on that of the
entomologist and helminthologist, and frequently he rejects out of hand
the valuable evidence provided by the parasitologists.

The fleas, unlike the feather lice, have only been associated with
birds for a few hundred thousand years (see p. 90), and through them
we can study quite another aspect of parasitism — namely the effect
on the parasite of the change to a new type of host.

In the following account of the Mallophaga and the Aphaniptera
we have concentrated on the British fauna, but it must be realised that
numerically the two groups are not comparable, for the former contains
about 1,500 species in Britain, and the latter about a baker's dozen.
Consequently, while it is quite possible to give a very brief account of
the various species of bird fleas, the feather lice have to be treated in a
more general manner.

'* The intromittent organ of fleas is probably the most complex
genital apparatus to be found in all insects.'*

CHAPTER 7

FLEAS (APHANIPTERA*)

{d(f)avT]S='NOT APPARENT, 7rTepoV=WING)

Though this little Creature is almost universally known
to be a small brown skipping Animal, very few are acquainted
with its real Shape and Figure, with the Structure, Strength,
Beauty of its Limbs and Parts, or with the Manner of its
Generation and Increase.

Dr. Hooke

Structure, Life-History and Habits

THE SIMPLEST way to collect bird fleas is to take a nest from which the
fledgelings have recently flown and to keep it in a cardboard box
or linen bag. Providing the nest is damped periodically, the larval or
pupal fleas continue to develop in the debris or rubbish in the bottom,
and in due course hatch out. It is a more lengthy process to collect
them off the bodies of their host. Less than one bird in ten harbours
fleas, and then generally only one or two specimens at a time. More-
over the host has to be enclosed in a receptacle immediately after being
shot or captured, otherwise the fleas hop ofl'and escape. The maximum
number recovered from a bird is 25 specimens from a house-martin.
On the other hand, no less than 4,000 have been bred out of a single
martin's nest.

On opening the collecting bag the fleas can often be observed
sitting at rest on the sides (Plate XXXIII). In profile they are faintly
reminiscent of miniature brown pigs — "bunch backed like a hog." This
effect is produced by the absence of a well defined neck, for the head
appears to pass broadly into the thorax. Moreover the flea is devoid of
a "waist," which is such a characteristic feature of wasps and many flies.

The largest British flea is the mole flea [Hystrichopsylla talpae) which
measures about 5 to 6 mm. in length. The British bird fleas vary from

* Also known as Siphonaptera
61

62 FLEAS, FLUKES AND CUCKOOS

if to 4 mm., the largest being the rock-dove flea {Ceratophyllus columbae) ,
although both the sand-martin flea {Ceratophyllus styx) and the moorhen
flea [Dasypsyllus gallinulae) come very near it in size. At the other end of
the scale we have one of the house-martin fleas [Ceratophyllus rusticus)
and the house-sparrow flea [Ceratophyllus fringillae) .

Fleas vary in colour from almost black to pale brown. Their integu-
ment is extremely tough and slippery, as anyone knows who has tried
to squash a flea in his fingers. The insect generally manages to squeeze
under a nail and make good its escape with a disconcertingly sudden
jump which the eye cannot follow.

It is, of course, well known that the hard part of an insect is external.
In other words the skeleton consists of a chitinous outer covering to the
body similar to that of a crab or a lobster instead of an internal scaffold-
ing like the bones of mammals and birds. This hardening and toughen-
ing of the cuticle is most pronounced, on the whole, in parasitic insects.

If a flea is examined under the microscope it is found to be covered
with strong, rather widely spaced bristles, arranged in definite rows or
groups, varying in length and thickness, and lying close to the body.
This greatly adds to the general streamlined effect. Each of these bristles
is set in a socket (Plate XXXIIIc) and articulates with the cuticle. They
are very valuable characters when it comes to classifying the fleas.

On certain segments the hardened exo-skeleton is produced into a
series of spine-like backwardly projecting teeth, which form combs
(Plate X). These combs greatly facilitate the animal's progress
through fur and feathers and protect vulnerable areas of their bodies.
Parasitic insects from quite unrelated groups which live in the fur of
mammals, such as modified flies (Nycteribiidae) and bugs (Polyctenidae)
parasitising bats, and the beetle [Platypsyllus castoris) from the beaver
have also developed comb-like structures. A few of the feather lice have
somewhat similar devices formed from expansions of the cuticle. This
type of comb is only found on parasitic insects. The genal comb
(Plate Xb) which protects the mouth, and the pronotal comb situated
on the first segment of the thorax are generally the most conspicuous
in fleas.

The head of the flea, as in all insects, encloses the brain and bears
the mouth parts, eyes and antennae. It varies considerably in shape,
and in the fleas which have become "fixed" such as the hen stick-
tight flea [Echidnophaga gallinaceus) and the parrot stick-tight flea
[Hectopsylla psittaci) the front of the head is sharply angled. This

FLEAS 63

facilitates their close, and in the case of the female, permanent attach-
ment to the host by their mouth-parts. A similar modification (Plate
XI), but less pronounced, can also be observed in the common
rabbit flea {Spilopsyllus cuniculi) which is partly sedentary, and in the
related shearwater flea {Ornithopsylla laetitiae).

Fleas are descended from winged ancestors (see p. 73) and the
thorax still bears a strong resemblance to the thorax of flying insects.
It has become secondarily adapted to support the jumping legs of the
flea. It consists of three segments which are broken up externally into
different sized chitinous plates thus giving it the appearance of a sort of
crazy pavement. In the hen stick-tight flea, and the parrot stick-tight
flea, the thorax is greatly reduced and the three segments are narrow
and crowded together. These fleas have lost the power of jumping and
consequently there is a corresponding reduction in the huge muscles of
the thorax.

The respiratory organs of a flea consist of a network of tubes, which
end blindly, known as the tracheal system. The air enters through the
external openings, the spiracles, which are conspicuous features along
the sides of the body, and is carried to all the tissues by the ramifications
of the tracheae.

In certain sedentary fleas, the spiracles on the thorax have been
lost and are now represented by mere pin-point depressions in the
cuticle, while those on the abdomen are greatly enlarged.

The chitinous external portions of the spiracles are, of course, rigid,
but just below the surface is a complicated apparatus whereby the
tubes may be shut. A rhythmical opening and closing of the spiracles
can generally be observed, which is associated with the inflation 01
deflation of the main trunks of the tracheal system. Sometimes when the
flea takes a lot of exercise, or is ripening eggs, the first and eighth
abdominal spiracles, which are much larger than the rest, remain open
continuously.

This type of respiration is obviously quite different from that of
vertebrate animals such as birds or mammals. Human beings are apt
to regard their own personal structure as "normal" and everything
that differs from it as distinctly humorous. It is difficult for them to
realise that fleas breathe through holes in their sides, have a nerve cord
below their stomachs and a heart in their backs; or that certain other
arthropods lay eggs through their elbows, urinate through their heads
and regularly practise virgin birth.

64 FLEAS, FLUKES AND CUCKOOS

The abdomen of the flea consists of a series of segments each of
which is protected, externally, by a dorsal and ventral overlapping
chitinous plate known respectively as thGtergum dindsternum(?\2itGXVIl).
The first sternum is missing, and the three last segments are highly
modified in connection wdth the sexual organs and form a series of flaps
and levers and struts of peculiar complexity.

The abdomen contains the digestive and excretory organs, the heart
and circulatory system and also the ovaries and testes. The main
nerve cord runs along the ventral side of the body and has, in addition
to the brain, a series of swelHngs at intervals along its length. These
swellings (see Plate XVII) are nerve centres known as ganglia. In the
male flea there are eight such nerve centres and in the female only
seven. This fact does not suggest that the male is the more gifted of the
two — on the contrary, a fusion of the gangha indicates a more highly
specialised or "advanced" condition. Apart from this curious form of
sexual dimorphism the internal structure of a flea is rather generalised
and presents no very unusual features. For further details the reader
is referred to the excellent descriptions of the anatomy of insects which
can be found in Ford's and Imms' books in the Mw Naturalist

series.

In many insects the male can be described as the weaker sex and
this is certainly true in the case of fleas. The female is larger, lives longer,
weighs twice as much and is hardier and more resistant if conditions
deteriorate. It is also said to assume the active role in mating. This last
point is difficult to prove and indeed is probably a subjective impression
due to the greater size of the female which in mating adopts a position
covering the male. When a male bird flea approaches a female it can
be seen to cock its antennae out of their grooves, and in view of the
important role these organs play in mating this might well be described
as taking the initiative. The ancient writers thought the antennae of
fleas were ears and it is of course quite possible that with them the flea
perceives vibrations. They may also serve as organs of smell and touch.
In bird fleas and their aUies they are much larger in the male sex and
when cocked are held aloft like a pair of horns (Plate Xld). During
copulation the male takes up a position beneath the female and uses
the antennae to grasp her firmly from below. At other times they
are folded back neatly into the grooves along the sides of the
head, thus adding to the general streamHned effect of the body
(Plate XI).

FLEAS 65

In the case of the hen stick-tight flea, which is sedentary, copulation
often takes place between adjacent individuals, without either of them
detaching themselves from the skin of their host — although the male is
not permanently fixed hke the female. The process may last twenty-
five minutes or longer.

It is easy to tell the sexes apart even without the aid of a hand lens,
as the end of the body of the male has a rather rakish upward tilt —
somewhat reminiscent of a drake's tail — whereas the female's body
merely narrows terminally. The external sexual organs or genitalia
are of primary importance in distinguishing between closely related
kinds, or species, of fleas. In fact among the bird fleas it is sometimes
the only practical way of telling them apart. These organs in the
male are fantastically complicated. The terminal segments are
modified for grasping the female, and the penis with its guiding
rods is itself a structure of extraordinary complexity — in fact it is the
most complex genital organ to be found in any insect. The more
one considers it, the more difficult it is to understand how such a
structure can have been evolved either by a series of mutations or by
natural selection, or by means of both. We have tried to understand the
way in which this apparatus worked from studying permanent prepara-
tions of copulating martin fleas, and we have puzzled over the sUdes for
hours. An American morphologist attempted the same study with
another species of bird flea. Although he elucidated many obscure
points much remained a mystery; he concluded his description with a
sentence which exactly expresses our views. " Truly," he wrote, "the
thing does not make sense."

The genitalia of the females are much less compHcated but they
also afford a most important clue to classification and relationship.
The female flea has the capacity of storing the male sperm, and
releasing it at intervals as her eggs ripen. This enables her to lay
fertilised eggs as long as two months after copulation. The internal
organ which receives and stores the sperm from the male, the recepta-
culum seminis or spermatheca (unpaired in all British bird fleas) is
chitinised and thus visible from the outside in cleared and mounted
specimens (Plate XVII). In outhne it roughly resembles a barrel-
shaped flask with a thick neck. The subtle diff'erence in the proportions
of these two parts affords the simplest character for distinguishing
between the females of closely related species (Plates XIII and XIV).
In Britain where one is concerned with relatively few fleas, it is easy

56 PLATE XIII

REGEPTACULUM SEMINIS OF BRITISH BIRD FLEAS
AND MAMMAL FLEAS

(x 165)

Ceratophyllus garei Cnatophyllus borealis

(from carrion-crow) (f^om rock-pipit)

Monopsyllus sciurorum Ceratophyllus columbae

(from red squirrel, for l^om rock-dove)

comparison with a and b)

Hoplopsyllus glacialis Ormthopsylla laetitiae

(from Artie hare; not British, (from puffin)

for comparison with/)

Dasypsyllus gallinulae Omeacus rothschildi

(from skylark) (from house-martm)

A^^n

""tl

1. .4

V"' t .-^ ■

t^i^^ml %

male XIII

Arthur L. E. Barron

PlaU XIV

PLATE XIV 67

RECEPTACULUM SEMINIS OF BRITISH BIRD FLEAS
AND MAMMAL FLEAS

(x 165)

a b

Ceratophyllus gallinae Ceratophyllus fringillae

(from blue tit) (from house-sparrow)

c d

Ceratophyllus farreni Ceratophyllus rusticus

(from house-martinj (from house-martin)

' f

Ceratophyllus hirundinis Ceratophyllus styx

(from house-martin) (from sand-martin)

FFC— F

g h

Monopsyllus anisus Ceratophyllus vagabunda

(from brown rat; not British, (from herring gull)
for comparison with a-h)

68 FLEAS, FLUKES AND CUCKOOS

enough to carry these differences in one's head and, once under the
microscope, there is Httle more difficulty in "spotting" species of fleas
than species of butterflies.

In nature bird fleas probably copulate when the host is incubating
eggs or when the young are in the nest or on the host itself, for they
seem to require not only a blood meal but a certain degree of warmth
to stimulate their interest in the opposite sex. In a glass tube they
remain completely indifferent until the tube is heated in the palm of
the hand. They will then mate readily enough.

Some fleas seem to require a meal from their true host before they
will copulate. In the laboratory the common rat flea [Nosopsyllus
fasciatus) will feed more readily on man than on rats but according to
Strickland this does not provide an adequate stimulus. The common
hen flea [Ceratophyllus gallinae) however, which is very hardy and less
particular in more ways than one, will breed successfully on mammalian
blood, man or rat. Some of the house-martin fleas copulate without
a feed at all — a fact which we have observed ourselves.

Many male fleas die soon after mating, but the female survives, not
only to deposit her eggs but to supply an important element in the diet
of her offspring. It has been proved that she requires a blood meal
before laying fertile eggs and therefore in the absence of the host
breeding is impossible. Blood appears to have a stimulating effect upon
the reproductive organs of the female, for she generally lays within
twenty-four hours of feeding even if she has been starved for weeks
previously.

In countries with well defined seasons, most phases of an insect's
life-cycle are restricted to certain periods of the year. For example
the purple emperor butterfly is only seen on the wing in June and July,
and wasps are not troublesome round the Christmas tree. Fleas are also
more in evidence at certain seasons. For example, in temperate
climates such as our own, the number of fleas per rat rises in the summer
and falls off sharply in the winter, whereas in parts of tropical India
the opposite is true and the flea population is at its height in the so
called cold season. In Texas the hen stick-tight flea almost vanishes
after the spring rains, but is again plentiful in dry cool periods in the
autumn. Pliny, many hundreds of years ago, remarked upon these
seasonal fluctuations and drew attention to the "fleas which skip
merrily in summer time in victualling houses and inns, and bite so
shrewdly."

FLEAS 69

Frequently both adult and larval fleas are found pullulating in the
nests of hibernating mammals. Brumpt states that a certain Cerato-
phyllus found in the nests of hibernating voles, lays eggs and breeds
right through the winter. If this is true the host's long sleep must be
troubled by bad dreams. Certainly during the period in which the
hedgehog is torpid, its fleas are quite active. It has been shown how-
ever that the rhythmical inflation and deflation of the tracheal tubes —
in other words the flea's breathing — is considerably slowed up during
the hibernation of the host. The quickest rhythms are found in gravid
females in summertime and therefore it seems likely that this species at
any rate does not breed in winter.

Bird fleas have a more sharply defined breeding season than mam-
mal fleas. Although in all species seasonal changes in climate affect the
number of eggs laid, the proportion which hatch and undergo meta-
morphosis, the duration of each larval stage and so forth, yet broadly
speaking, if conditions are reasonably favourable, rat fleas and many
other mammal fleas are known to lay eggs, even if reduced in number,
and breed all the year round. But the conditions such as plentiful blood
meals and a raised temperature which induce the common rat flea and
the stick-tight marsupial flea {Echidnophaga myrmecobii) to breed in mid-
winter in the laboratory, have no effect on the common hen flea which
will only lay eggs in the spring or early summer. This indicates that the
parasite is well adapted to its particular hosts. It is vital that the flea's
life-cycle coincides with that of birds, for it is only during a brief
period in the spring that the host occupies a nest.

In India the native jungle fowl {Callus gallus) is not infested with
Ceratophyllus gallinae. This flea is undoubtedly a parasite of European
wild birds which has only fairly recently developed a marked pre-
dilection for the domestic fowl. Although birds are present all the year
round in hen houses Ceratophyllus gallinae still retains a definite spring
breeding season. In time this may be modified to suit the new condi-
tions. Here the stage is set for the evolution of a new physiological race
and possibly a new species.

Some permanent parasites like the feather lice, pass their entire
life-cycle on their host. It is of supreme importance to them that their
eggs should not fall off' after they are laid. To ensure against this mis-
fortune the female glues them individually and with extreme eflficiency
to the feathers (Plate XXIV). In the case of the flea, which has a
free larval and pupal stage generally spent in the nest, the reverse is

70 FLEAS, FLUKES AND CUCKOOS

true, and if the eggs are laid on the host it is preferable that they
subsequently roll off.

Like birds themselves, different species of fleas lay differently
shaped eggs. The human flea [Pulex irritans) has a nearly spherical
^gg, but those of the common hen flea are elliptical. The eggs of the
tropical rat flea {Xenopsylla cheopis) are midway between the two. In
colour they are pearly white and relatively smooth with rather soft
shells which are easily dented. They are devoid of the elaborate
sculpture and ornamentation which adorn the eggs of butterflies and
many feather flee but under a high power magnification the surface is
seen to be finely pitted. When the host scratches and preens itself they
roll off and are conveniently scattered. A keen entomologist once
collected a spoonful off the lap of a visitor who, during tea, was affec-
tionately fondling his kitten. Often the eggs are deposited directly in
the nest of the host. They are just visible to the naked eye and are
faintly reminiscent of a fine dusting of castor sugar. A female flea, at
intervals, deposits a total of between 300 and 500 eggs. Except in the
case of a sedentary species they are laid singly or in small batches —
during the day and night — either on the host or on dried twigs and
leaves in the nest. The sedentary species sometimes lay small tgg
masses, in which the individual eggs are glued together.

The hen stick-tight flea expels her eggs forcibly and they fall well
clear of the head of the host on which this species congregates. Accord-
ing to the temperature and humidity they hatch in 2 to 14 days.

All but five of our sixteen bird fleas belong to the genus Cerato-
phyllus and these are essentially fleas of temperate cHmates. Especially
in the early stages of their life-cycle they require a cool humid atmo-
sphere.

The eggs of the common rat flea, which is fairly closely related to
the bird fleas and until recently was included in the genus Ceratophyllus,
hatch at a temperature of 41 °F. The eggs of the tropical rat flea,
however, require temperatures above 54°F. before the larvae can
emerge. Hirst, discussing the problem of bubonic plague and its flea
vectors, remarked that in all probabihty each species of rat flea has
adapted itself to some particular range of climatic conditions. This is
also undoubtedly true of bird fleas and it of course includes adaptation
to the ranges of humidity and temperature found in the various types
of nest they infest. It is obvious that conditions in a gannet's nest, a
sand-martin's nest and a starling's nest are very diflferent. The

FLEAS 71

hen stick-tight flea dies in the larval stages if the temperature falls
below 50°F. Our poultry is thus saved in this country from a serious
scourge.

The flea larvae rip up the egg shell, which generally cracks longitu-
dinally, with a spine situated on the front of the head. When they
emerge after about ten minutes' wriggling they are minute cylindrical
semi-transparent maggots adorned with a few hairs but without eyes
and with merely a pair of anal struts on the last segment to serve as
appendages (Plate XVIII). Some species are very much more hairy
than others. They twist about actively in the nest debris and some-
times curl themselves up sharply like a watch spring. It is especially in
this stage that fleas require a humid atmosphere. Even the sweat and
urine from the host's body play a large part in keeping the larvae
alive. They cannot survive dry heat. Feather lice which pass their
early stages on their hosts are independent of external climatic changes
and their situation in this respect is singularly secure compared with fleas.

Buxton once measured the relative temperature and humidity in a
Palestine cow-shed and two rat holes opening into it. The temperature
recorded was the same in all three spots, but the greater humidity in
the holes was sufficient to make the development of the flea larvae
possible within them. No doubt it is the moisture requirements of the
larvae which has imposed one of the greatest barriers to the infestation
of birds by fleas. For insects such as these the change from a mammal's
humid nest or lair to the dry aerial home of birds is revolutionary. It is
significant that most of the existing bird fleas are found on species which
breed on the ground and in banks, or use mud freely in the construction
of their nests.

According to the temperature and humidity, which may speed up
or delay metamorphosis during all its phases, the larval stage of a flea
may last from one to twenty-four weeks. During this period it moults
three times. (There are a few exceptions among the sedentary species
which have only two moults.)

It is an undisputed fact that the mouth-parts of the larvae of fleas
are adapted to gnawing but their diet has been the source of endless
discussion. Leeuwenhoek as far back as 1694 noticed larvae of the
pigeon flea "red with blood" but subsequent writers maintained that
this element did not form part of their normal food. On the contrary,
they were said to maintain themselves on organic refuse such as the
dung of their host, dead flies, the bodies of adult fleas and the sawdust

y2 FLEAS, FLUKES AND CUCKOOS

in used spittoons. Aristotle was quite ignorant of the life-history of the
flea but he had observed that dung was a contributing factor to their
welfare. He wrote, "Fleas are the result of putrefaction of smaller
bodies, for example where dried dung is, there you find fleas." One
early naturalist reared the larvae on "the bran hke substance which
sticks in the comb when puppies are combed." It appears that this
unattractive diet is adequate for the larvae of the tropical rat flea and the
human flea but not for all species. Sharif proved that in addition to organic
refuse which forms a necessary part of its diet it is essential for the larvae
of the common rat flea to eat small quantities of blood. In nature this
is provided by the female flea which, during her interminable meals,
squirts out quantities of undigested blood through the anus, and thus
amply justifies her Gargantuan appetite.

It was also proved experimentally that it is impossible to rear
larvae successfully if the iron content has been extracted from the blood
fed to them. One wonders if, in some cases, the blood-sucking habit of
insects was acquired in connection with a lack of iron in their diet.
This substance is essential to their normal growth and development,
and a new source of supply may have conferred an immeasurable
advantage on the pioneers who first tapped it accidentally.

It is, however, most unusual for an insect to require blood during
more than one phase of its life-cycle and in this way, as in so many
others, fleas are peculiar and exceptionally interesting. " Her young
ones also suck up blood." In the case of the common house-martin flea
[Ceratophyllus hirundinis) and the common hen flea it is known that their
larvae thrive best on food which contains excrement and blood drop-
pings of their parents, but it appears that at a pinch they can be reared
successfully on broken down feather sheaths and epidermal scales.

The larvae of fleas sometimes swarm in thousands in one nest.
It is therefore not surprising that they are occasionally found on the
bodies of nesthngs. Twenty per cent, of sand-martins are said to be
infested during the nesting season. No doubt if they could evolve a
closer relationship with the host at the larval stage their lives would be
less hazardous and bird fleas as a whole might, Hke the feather Hce,
become more successful in the walk of life they have chosen.

The larva spins itself a cocoon before pupating. This is attached to
twigs in the nest, and since grains of sand and dirt adhere to the outside,
the camouflage is most efl^ective. There is a certain amount of specific
variation in the structure of cocoons. Those of the common hen flea

FLEAS 73

are pure silk, very strong, densely woven yet soft, and pale brown in
colour.

The pupa itself vaguely resembles the adult in shape. Its head,
body and legs, held close to its sides, can be made out, and in fact it
suggests a wax model of a flea made by a rather indifferent artist.
One of its most fascinating features, clearly visible in the pupa of the
common hen flea though not in all species, is the vestigial wing buds on
the thorax. They represent the only concrete evidence that fleas are
descended from winged ancestors — a fact most entomologists inferred
years before these structures were demonstrated by Sharif.

This stage of the life-cycle may last two weeks or more than a year.
Long after the flea is fully developed it can lie dormant within the
cocoon (Plate XVIII) waiting for some outside stimulus to precipitate
hatching. It then bursts out within a spHt second. The vibration
caused by the footfall of a passing animal may be sufficient.

After emerging from its cocoon a flea can live for a considerable
time without feeding. In this stage both sexes survive for about the
same period. Providing they are kept in rubbish, adults of the common
rat flea can live without food for seventeen months in captivity. In the
case of well fed fleas which are subsequently starved the females live
nearly twice as long as the males. On a full diet of human blood the
human flea has survived 513 days and the common hen flea 345 days.
A Russian Ceratophyllid, however — a true hero of the Soviet Union —
is said to have lived 1,487 days ! In captivity, however, fleas, Hke their
hosts, probably survive much longer than in nature. It is not unusual,
for example, for an adult robin to attain 10-12 years in an aviary,
whereas only about one year is the average expectation of life in the
wild. Hirst found that in soHtary confinement a flea lived twice as
long as in the company of others and it seems probable that in nature
they have a short life and a merry one.

The food of an adult flea is blood. Accordingly the mouth-parts
have been transformed into a piercing and sucking apparatus (Plate
XII). In Ford's book in the New Naturalist series there is a very fine
description of the mouth-parts of a relatively primitive insect (a cock-
roach) which shows how these have been modified in butterflies to form
an apparatus for imbibing nectar from the centres of flowers. In fleas,
however, it is no easy matter to decide which portions are homologous
with those of the primitive biting types, and the experts are by no means
agreed upon this question.

74 FLEAS, FLUKES AND CUCKOOS

The wound in the host's skin and flesh is inflicted by the maxillary
lacinia (Plate XII b) — a pair of sword-hke blades which bear four rows
of upwardly projecting teeth on their outer surface. Running along the
middle of the inner surface is a gutter or channel. Down this, saliva,
containing an enzyme which inhibits clotting of the host's blood, flows
into the wound. While feeding, a thin median unpaired rapier-like
blade, the epipharynx, lies squeezed between the two maxillary blades —
all three together forming a tube up which the blood is drawn by the
pumping mechanism in the head. The labium serves to protect the
lacinia and bears the labial palps which are apparently organs of touch
and are used as such when the flea is selecting a good spot on the host's
skin through which to drive the blades. When a flea is feeding the
mouth parts become fully embedded in the flesh, the head is drawn
down on to the skin of the host, the front legs are tucked back or some-
times flexed and held above the body (see Plate XXXIII), and the flea
supports itself with the middle and back pair, or only the latter. It is
thus tilted sharply forward and appears to be standing on its head or in
the early stages of turning a somersault. In the case of the hen stick-
tight flea the feeding position is somewhat different. The maxillae stick
out in front rather like the proboscis of a tick only not so straight — no
doubt a more suitable attitude for a sedentary species to adopt.

Fleas have a voracious appetite and they have been known to feed
for four consecutive hours without a pause. The tropical rat flea which
is a particularly fierce feeder, weighs only 0.6 milligrams (or i /40,ooo
of an ounce) and the capacity of its stomach is 0.5 cubic millimetres.
Only a mere fraction of the blood imbibed is digested. Most of it
passes through the flea unchanged and is squirted out drop by drop
at the hind end or anus.

Many beginners, when first examining a mounted and cleared
specimen of a flea, have been puzzled by what appears to be a strange
patch of bristles in the forepart of the abdomen (Plate XVII). These are
in reality a mass of about 800 spines in the inside of the crop or proventri-
culus — the only highly specialised portion of the alimentary canal of a
flea — which help to crush up the blood corpuscles of the host.

It is not known if the non-sedentary species of bird fleas have any
favourite feeding spots on the host's body. Rat fleas generally try to get
a hold between the shoulder blades or on the back of the neck where it
is more difficult for the host to kill them. Many wild rodents such as
marmots are more frequently bitten on the rump. There is also a

FLEAS 75

great variety in the feeding habits of even closely related species of
fleas. Some tend to take short frequent meals, others long feeds at
considerable intervals. Some, like human beings, lose their appetites
in hot weather. Again, one species will bite immediately it comes into
contact with the host, and another will wander about trying here and
there before it finally settles down to feed.

The tropical rat flea is a wary flea and is easily disturbed, but on the
other hand it will try again and again to get going, whereas Xenopsylla
astia, a closely related species, if once put off or distracted, temporarily
refuses to bite.

It is true that most fleas are not so closely bound to their host as are
the feather hce, but although they are in a sense free they have little
or no possiblity of actively searching for a bird, and luck must often
play a considerable part in finding one. It is therefore fortunate for the
flea that it is endowed with the power of fasting for considerable
periods. Nevertheless, it must be the fate of a large proportion of bird
fleas to hatch out in a nest long after the birds have gone, and to perish
miserably without the hope of ever tasting blood.

Little is really known about the senses of fleas, but it appears that
where the response to a host is involved they only function when the
animal is at close quarters. For example, if hungry rat fleas are intro-
duced into a cage with a rat, they do not, as would be expected, make
a bee line for it. Instead they wander about in an aimless manner until
their random movements bring them within a few inches of the host. Only
then will they make directed efforts to reach the animal. Nevertheless
in practice this method is evidently rather effective, for if the cage is
opened after a few hours, most if not all of the fleas will be found on the rat.

During the Plague Commission's investigations in India and Egypt,
guinea-pigs were sometimes liberated in plague infested buildings
where rats had been known to die of the disease. Within several hours
they had collected scores of rat fleas, and in turn became infected with
the plague. As many as 988 fleas were caught off* one guinea-pig. All
investigators, however, have not recorded similar successes with these
living traps. Some unknown factor, such as weather or temperature,
seems to affect the appetite of the fleas or their capacity or inclination
to wander about and find a new host in this manner, and sometimes the
guinea-pig did not collect a single specimen.

The females of several species of fleas are sedentary and after finding
a suitable host, they collect on its head, either on the ears or in the

^6 FLEAS, FLUKES AND CUCKOOS

nostrils of mammals, or round the eyes and wattles of poultry. They
then fix themselves by means of their mouth-parts, which become
embedded in the skin. When these fleas, male or female, first reach
their host they begin to travel against the lie of the fur or feathers.
Sooner or later this inevitably leads them to the head (occasionally
they take a wrong turn down a leg and finish up between the toes), and
when the ears or wattles are reached the shortness of the hair or paucity
of feathers no longer produce the feeling of resistance to which the fleas
apparently respond, and the females stop moving and fix themselves.
It would be interesting to see if shaving a small ring of feathers, say at
the base of the bird's neck, would trap the fleas into settling within
easy reach of the host's beak.

It seems highly probable that smell exerts a strong influence on the
flea's choice of hosts. It is a well-known fact that not only are horses
immune to their bites, but also the grooms who look after them.
Apparently no attempt has been made to exploit their dislike of horse
smell, and there does not appear to be a commercial insecticide or
deterrent with the attractive odour of stables.

Russian workers claim that fleas have a strong sense of smell and
that at a distance of 8 cm. (about 3 inches) they can distinguish between
the effluvia of a hedgehog and a mouse, and are also guided back to the
host's nest by its odour.

The field-mouse flea (Ctenophthalmus ag^rtes) even when starving, will
only bite man with the greatest reluctance. There is obviously some-
thing repellant about him, as far as this flea is concerned, which exerts
its influence long before the question of taste comes into play. It is
probably smell.

Fleas are attracted to warmth, and there is a certain temperature,
generally around that of the host's body, which they prefer and con-
sequently seek. Once a cat flea has found a cat it has also found the
conditions in which it is most comfortable and its wanderlust vanishes.
It therefore remains on the host. Certain parasites, such as ticks, only
feel an urge towards high temperatures when they are hungry. Once
gorged they drop off' the host's body. Bird fleas (which, unlike cat
fleas, spend most of their time in the nest) may also find the warmth
of the host unattractive after they are fully fed and so withdraw into
the nests. However, no experiments have been performed to test this
theory.

Many fleas are bUnd but aU the British bird fleas have eyes placed

FLEAS 77

on either side of the head near the anterior edge of the antennal
grooves. Although the eyes of the fleas are situated laterally, they are
in fact displaced dorsal ocelli. These relatively simple organs probably
do httle more than enable their owners to perceive the difference
between Hght and darkness and thus would only assist them in finding
a host if it were in their immediate vicinity. Bird fleas are photonegative,
that is to say, other things being equal, they move away from light.
If, however, a collecting box or container is opened suddenly, the fleas
inside often begin to crawl towards the aperture, for their attraction
to the source of air currents is very marked and is apparently stronger
than their aversion to light. As Strickland pointed out they become
greatly agitated if blown upon. This reaction no doubt considerably
assists them in finding a host which may be moving about or breathing
in their vicinity. It has been suggested that the pygidium (Plate XIX)
or sensilium, is an organ connected with this particular reaction. This
is an extraordinary saddle-shaped structure which is present in both
sexes, situated on the dorsal surface near the terminal end of the
body. Its surface is densely clothed with spicules, and honeycombed
with widely spaced pits, from the centre of which arises a single long
sensory brisde. From above these pits appear like small rosettes
(Plate XIX). A few experiments have been performed in Russia and
Germany to test whether the pygidium is in fact connected with any
particular sense. It is claimed that if this organ is painted over or
cauterised the fleas cannot perceive air currents and consequently fail
to find a host. An American entomologist once tried tickling the
pygidium of feeding fleas and he recorded that they showed no visible
response. This, however, is scarcely a fair test, since fleas, Hke some of
their mammalian hosts, seem marvellously insensitive to outside
stimuH once their attention is focused upon a hearty meal.

It has already been pointed out that the adult flea is totally devoid
of wings. Therefore unUke certain other parasites, for example the
mosquito, it cannot fly in pursuit of its host. The jumping legs of the
flea are, however, very powerful and to a certain extent are good
substitutes for wings.

In 1910, Mitzmain, an American naturahst, measured the leap of a
flea and found it could cover a distance of thirteen inches horizontally.
This was believed to equal a 300 yard jump by a six foot man. At the
end of the last century Rothschild observed "performing" fleas at a
circus moving objects many times their own weight, and was greatly

78 FLEAS, FLUKES AND CUCKOOS

impressed by their enormous strength. He considered the feat equiva-
lent to a man dragging two full sized elephants round a cricket ground.
The modern physiologists, as Imms has pointed out, take another view.
They hold that as the body of an animal becomes smaller so the relative
(not the absolute) power of a muscle increases. The great strength of a
flea is therefore more apparent than real, and according to present day
calculations the feat of the performing fleas would be compared with
greater accuracy to a man pulling two sheep round a cricket ground.

The structure of the legs has been especially studied in fleas from
the sand-martin. There is a broad flat coxa (hip) joined by a small
joint called the trochanter, to a short stout femur (thigh) and tibia (shin),
and an elongated five-jointed tarsus (foot). The pair of claws on the
fifth tarsal segment do not, at first sight, appear to be particularly
powerful, but they are nevertheless marvellously well adapted to
clinging.

As we have already pointed out, the bristles and spines lie close to
the flea's body, almost like scales on a fish. Those on the feet, however,
stick out at an acute angle (Plate XXXIIIc) and act as grappling
irons. Anyone who has attempted to transfer fleas from one tube of
alcohol to another with the aid of a paint brush, cannot fail to be
impressed by the manner in which even a dead flea hangs on to hair
or bristles.

Fleas can also climb up a vertical glass plate as long as the surface
is moist. On a dry, clean, glass surface they cannot keep a foothold and
fall off after reaching a height of a few inches. All fleas seem to show a
desire to climb upwards, away from the ground. This reaction, which
is called negative geotropism, may also help them in finding a host.

The human eye is not sufficiently quick to see the action of a flea's
leg when it actually jumps. Some writers believe that the only move-
ment is a sudden straightening of the leg, and its extraordinary force is
due to the simultaneous extension of both the femora and tibia. Possibly
owing to the fact that the hind end of the body is heavier than the head,
a flea turns over in mid-air and lands facing the way from which it
came. It is the back legs which touch the ground first and take the
impact of landing.

Anyone who has bred fleas and watched them, knows that they
react to various stimuli, such as air currents, vibrations or touch, by
apparently random leaps. In this way they no doubt escape from
certain enemies and also in other cases may reach a passing host. As

FLEAS 79

Waterston remarked, " It is more than likely in a life so precarious as a
flea's speculative jumping plays a very large part."

In many insects one sex, generally the male, hatches out before the
other, but in the case of fleas it is the female which emerges first. The
period it spends in the cocoon is shorter than that of the male. As it
also outlives the male by many months and can withstand spells of
adverse conditions to which the male promptly succumbs, there are times
when a breeding population of fleas consists almost entirely of females.
Most large collections in the past were made off' mammals theniselves
and the large excess of female fleas sometimes observed was attributed
not only to the greater agihty of males which more often escaped
capture, but to a deep seated divergence in the habits of the sexes—
the females supposed to cling to the body of the host and the males to
remain in the nest. Indeed there is some experimental evidence to
suggest that the females are more closely bound to the host's body.
Quite recently it has been shown that the proportion of male and
female fleas on rats in certain cities in the U.S.A. varies according to
the weather. On hot days males predominate and on cold days females.
In the case of bird fleas, however, some excess of females is also found
when specimens are taken direct from the nests. Waterston recorded
2,368 (or 56 per cent.) females to 1,672 (or 44 per cent.) males of
C.farreni from house-martins' nests and Rothschild found out of a total
of 1,218 fleas (five species were represented) from house-martins' and
swallows' nests that 732 (60 per cent.) were females. In many parasitic
insects there is a very marked tendency for the sex ratio to tip more and
more sharply in favour of the females. The reason for this is obscure.
Thus the males of certain Hce have so far never been found. Although
female fleas lay many unfertilised eggs, these do not develop. How-
ever, as one male flea has been known to fertihse thirteen females
their activity makes up to a certain extent for their numerical
inferiority.

Because relatively few fleas are found on the bodies of the birds
themselves it is assumed that they spend the greater part of their time
in the nest or hiding in debris and only visit the host periodically when
they require a meal. There can be little doubt that the greatest danger
to a flea is the active and efficient defence put up by the host. It is no
mere coincidence that the hen stick-tight flea is only found round the
eyes and wattle of poultry— where the birds cannot preen diemselves
effectively.

80 FLEAS, FLUKES AND CUCKOOS

In the course of several experiments Buxton showed that out of
50 fleas placed on a captive mouse only approximately 14 survived on
the seventh day — the rest having presumably been eaten or killed by
the host. Undoubtedly birds destroy many fleas and their remains are
sometimes found in the host's crop. On the other hand there is no
evidence that they form part of the normal diet of any insectivorous
bird. Another point brought out by Buxton was the higher proportion
of fleas which survived on captive baby mice as opposed to those on
adult mice. Fledgelings are also relatively helpless in the face of attacks
by parasites and the various species which pullulate in their nests must
greatly reduce their strength and vitality.

By far the most uncomfortable nests are those of the sand-
martin. Ceratophyllus styx, which teems in thousands in their burrows,
over-winters either as an adult or as a pupa which hatches in the spring.
It is sad to think that when the sand-martin reaches its breeding haunts
in April, having successfully endured the hardships and hazards of
migration, it is met by a reception committee in the form of thousands
of ravenous fleas which can be seen waiting round the entrance to thenests.

It is perhaps obvious that one of the reasons why martins are
generally so heavily infested with fleas, both with regard to actual
numbers and variety of species, is because of this habit of returning
again and again to the same nesting site. Holes in mud banks or quarries
(Plate XXXV), and mud nests provide a favourable habitat for the
early stages in the life-cycle, but this reason alone is insufficient to
account for the numbers concerned. Compared with a house-martin
flea such as C.farreni, the species infecting warblers, finches and thrushes
have an extremely precarious existence. The temperature in a bird's
nest during the incubation period and the rearing of the young fledgelings
is sufficiently high to speed up metamorphosis of the flea to a maximum
degree. The number of blood feeds, temperature, copulation and fertile
egg laying are intimately linked and in the spring the flea population
must be seething with activity within the nest. These palmy days are
all too brief and at the end of 1-2 months the young birds are fledged
and leave the nest never to return. Maybe one or two fleas, busy
feeding on their host at the time, are carried away on each fledgeling.
The great majority, whatever stage they have reached in their develop-
ment, are left to perish miserably in the deserted nest.

On several occasions fleas have been observed leaving birds' nests
in large swarms, and in Russia migration from abandoned mammals'

FLEAS 8l

lairs is considered the rule. Although these mass movements have only
been noted rarely in Britain it seems likely that this type of migration
plays an important part in overcoming the hopeless situation of fleas
left in nests to which the hosts do not return. Scattered over a wider
area and able to fast for long periods, their chances of coming into
contact with a passing bird would be greatly increased. Fleas are
frequently noted in isolated situations apparently far removed from
either nest or host. For example there are records of two common
bird fleas, the hen flea and duck flea, collected from under stones, on
palings, under the bark of trees, among dried leaves, in hedge clippings,
in a pile of reeds, in moss, on rocks, in caves, in barns and even swept
from grass and flowers.

Up till now no observations have been made regarding bird fleas'
preference — if any — for either sex of the host. Collectors rarely take
the trouble to record the necessary data. Linnaeus declared that women
harboured more fleas than men, but male squirrels on the other hand
seem more heavily parasitised than females. Where only the hen bird
incubates the eggs, the opportunity of becoming infested with fleas is
obviously greater in her case.

In the butterfly collection varieties take a prominent place.
Individual fleas sometimes display variations which are just as remark-
able as, say, the black variety of the swallowtail, but so far they have
not attracted much attention. There are certain characters of fleas
which seem to vary more than others and in these — for example the
shape of the seventh sternite of the females — the arrangement of the
bristles is also variable. In fleas, as well as human beings, no two
individuals are exactly alike. The bristle formula on the abdominal
segments of a flea was worked out by Jordan who calculated that he
would require 14,482,000,000,000 specimens in order to be sure that he
had another one with the same arrangement on the sternites alone !
Varieties, however, are well worth studying, for in them one often
catches a glimpse of the future evolutionary tendencies in the species or
even the family concerned.

The Distribution of Bird Fleas

Any attempt at discussing the distribution of bird fleas must to a
certain extent prove futile, because of the general lack of coUecting.

82 PLATE XV

THE 8th STERNITE AND TERMINAL PORTION
OF BRITISH BIRD FLEAS

(x 75>)

a b c

Ceratophyllus rossittensis C. gallinae Ceratophyllus Jringillae

(from carrion-crow) (from goldfinch) (from house-sparrow)

d e f

Ceratophyllus borealis C. columbae Ceratophyllus garei

(from Arctic tern) (from rock-dove) (from duck)

Arthur L. E. Barron

Plate XV

Plate XVI

Arthur L. E. Barron

PLATE XVI 83

THE 8th STERNITE AND TERMINAL PORTION

OF BRITISH BIRD FLEAS

(X 75)

a b c

Ormacus rothschildi Ceratophylliis hirundinis OmithopsyUa laetitiae

(from house-martin) Cfrom house-martin) (from Manx shearwater)

d e g

C. rusticus C. vagahunda Cfarreni C. styx

(from house-martin) (from jackdaw) (from house-martin) (from sand-martin)

FFC— G

84 FLEAS, FLUKES AND CUCKOOS

Therefore, all the suggestions which follow should be regarded as
tentative. Despite the relatively large numbers of specimens taken from
Ashton Wold and Tring Park, these two places are not particularly good
spots for fleas. In this case, as in so many others, the distribution
shown is that of the collectors rather than that of the fleas (see Map 3).
Bat fleas apparently show a strong predilection for cathedral cities but
this does not reflect their sectarian views; it merely demonstrates the
fact that their hosts are more numerous and thus easier to catch in
large belfries than in smafl ones.

In studying the distribution of the fleas we are confronted with a
much more complicated problem than in the case of the feather lice.
Mallophaga pass their entire life-cycle on the bird and are so closely
linked to it that their own distribution closely parallels that of the host.
Whatever limits the range of the bird, whether it is chmate (past or
present), or food, or scarcity of nesting sites, or competition with other
birds, or geological history, these same factors limit the range of the
feather lice. They do not however exert a direct influence upon them.
The bird, not the external habitat, is their environment. In the
case of the adult fleas they are also closely hnked to the host, which
therefore must play an important role in determining their distribution.
However, the larval stages are free and are therefore influenced by all
the elements which aflect a free living organism. There are many
striking examples which illustrate this fact. The range of the hen
stick-tight flea, despite the wide distribution of the host, is restricted to
areas with a tropical or sub-tropical climate. The common rat flea
is rare or absent in the tropics and more or less confined to Europe.
Unlike its host it does not thrive in hot climates and has fafled to
spread aU over the inhabited portions of the globe with man and his
four-footed hangers-on. The rock-dove flea which is also a parasite of
the domestic pigeon, has not spread beyond Europe. The dovecots of
the United States harbour only hen fleas. In these cases the fleas fafl
short of the distribution of their host because the requirements of the
larvae limit them to certain ranges of temperature and humidity.

It has already been pointed out that many fleas are not host specific
and are found on a wide variety of birds. Nevertheless there is often a
preference for certain birds with similar habits, and thus the fleas in
question are distributed according to the conditions, or microclimes,
found in diff"erent types of nest. Let us take for example three of the
commonest bird fleas in Britain, the hen flea (C. gallinae) the moorhen

FLEAS 85

flea {D. gallinulae) and the duck flea (C. garei) (Maps 2, 3, 4). The hen
flea is apparently much more tolerant of the dry conditions found in
hen-houses and also in dry, loosely built nests placed in elevated situa-
tions. It is found more frequently than any other flea in the nests of the
sparrow, starling, sparrow-hawk, swallow and so forth. D, gallinulae^
however, prefers nests situated in relatively low positions such as those
of the robin and warblers. It also seems partial to the closely built nests
of finches, and in those of blackbirds and song-thrushes the relative
frequency of these two fleas is about the same. C. garei on the other hand
is essentially a ground flea, and can survive in wet swampy situations
which prove fatal to the other two mentioned above. Thus it is the only
one of these three fleas met with in the nests of ducks and geese, and
certain waders and sea birds. No doubt this type of distribution reflects
the larval adaptations of the fleas in question, and results in different
horizontal zones of distribution within the same locality. Birds them-
selves show marked habitat preferences and we do not find rooks
nesting on the ground or partridges in the tree tops.

There are certain cases where the distribution of the flea probably
closely parallels that of the host, but collecting has been so inadequate
that it is impossible to make any definite statement to that effect. The
common house-martin flea (C. hirundinis) is found in Europe and the
Himalayas and North Africa, and it seems likely that it accompanies
the bird throughout its range.

The house-martin is divided up into several geographical races or
subspecies. That is to say in certain areas where it is found the birds
show marked variations common to the population of house-martins in
that particular district. Thus an expert would be able to tell whether
certain house-martins had bred in Algeria or the Himalayas or North
Europe, by noting small differences in the colour, size, weight and so
forth.

There are two house-martin fleas, C. hirundinis and C. farreni, which
are known to extend their range beyond Europe. C. hirundinis, as we
have already explained, is found on all three subspecies of the martin,
but itself remains unchanged. At any rate there are no visible mor-
phological changes connected with its geographical distribution. We
have no method of estimating physiological differences which may be
present. C. farreni, however, has split into two subspecies — one in
Europe and one in North Africa. Only females are known from the
latter region but these show constant differences in the arrangement of

86 FLEAS, FLUKES AND CUCKOOS

the bristles and the shape of the seventh sternite. So far we know of no
explanation of the fact that one insect displays geographical variation
throughout its range and another, with the same host and the same
distribution, does not. However, it will be seen from the section on the
evolution of British bird fleas (p. 94) that these two species are not
very nearly related and C. hirundinis may be a much more recent acquisi-
tion of the house-martin than C.farreni. Time, and a certain degree of
isolation, is necessary for the estabhshment of subspecific differences in
a population of either fleas or birds.

An exceedingly interesting case is that of the sand-martin and its
fleas. These birds are found in Europe and the United States and
specimens from both continents are indistinguishable. The martins as a
group are considered to have originated in the Old World and to have
spread to the New World in Pliocene times. On the grounds that the
sand-martin in the U.S.A. is not sub-specifically distinct from the
European bird, it is argued that it may well have invaded the New
World at a much later date, possibly in post-Pleistocene times. When
we come to consider its fleas a most surprising fact emerges. The
European sand-martin flea (C. styx) and the American sand-martin
flea (C. riparius) although very closely related are specifically distinct.
It is irresistible to suppose that the American flea is an oflfshoot of the
European flea, although it seems strange that it should have been more
aflfected by the new environment than the host. It must be remembered
that the main population has to over-winter in the nesting site whereas
the host seeks more congenial quarters farther south. Therefore one
can imagine that winter in the flea's new habitat might be strikingly
dififerent — say colder, or wetter, or more prolonged, than in the pre-
vious winter quarters. This might lead to a speedier evolution of the
parasite.

Three important types of distribution are thus demonstrated by
the martin fleas. First, fleas which infest the host right across its
range of subspecies, but themselves show no geographical variation.
Secondly, fleas which show subspecific variation paralleling that of the
host. Thirdly, fleas which show either subspecific variation or specific
differentiation while the host itself remains unchanged.

A fourth type of geographical variation is, however, illustrated by
fleas. D. gallinulae, as we have already shown, is not host-specific and
is found on a very great variety of birds. This species has diverged into
sub-species without any reference to the hosts. Thus in the Western

FLEAS 87

United States we find one geographical race and in Europe another,
no matter what birds the flea happens to infest.

So far we have considered certain bird fleas which parallel the
host's range, and others which fall short of it. There are a few cases,
probably, where a bird flea has extended its range beyond that of the
true host, but these are, for obvious reasons, rather difficult to detect.
C. gallinae is possibly an example. There is some reason to think that
originally it was a tit flea, but on the domestic fowl it has invaded
remote islands where the tits are absent.

There are other aspects of this problem which appear still more
complicated and are more difficult to understand. We have for example
the two very closely related species of bird fleas C. garei and C. borealis,
which both favour ground nesting birds with a preference for wet or
swampy nesting sites. The former is distributed throughout the main-
land of Britain. The latter is confined to the outer western isles such
as St. Kilda, Inishtrahull and the Scillies where C. garei is absent
(Map 2). The explanation of such a distribution is obscure and one
can but hazard a guess. Maybe the factors are inter-specific competition
and C. garei^ a late comer, may have ousted C. borealis throughout the
mainland of Britain. The latter has only survived on outlying
islands, and on the continent, in the Alpine fastnesses of Central
Europe.

The distribution of C. vagabunda is also interesting although in view
of the collecting lacunae little can be offered beyond a few tentative
suggestions and speculations. This flea is rather rare and is apparently
an ancient species, and it has broken up into geographical races one of
which is pecuHar to Britain. It is chiefly an inhabitant of nests of rock
dwelling sea birds such as the herring-gull {Larus argentatus) and the
shag {Phalacrocorax aristotelis) . It has a Northern or Boreal distribu-
tion, and specimens are known chiefly from Spitsbergen, the Shetland
Isles and Outer Hebrides, Northern Turkestan, Northern Siberia and
Alaska. It is also found in the Alps of Central Europe. This is quite a
well known type of distribution and is believed to be the result of the
advance and subsequent retreat of arctic conditions during one of the
glacial periods or ice ages. There are similar examples among many
British plants and animals such as the small gentian {Gentiana nivalis),
the star saxifrage {Saxifraga stellaris), a butterfly, the mountain ringlet
{Erebia epiphron) and the alpine hare {Lepus timidus) and the ptarmigan
{Lagopus mutus).

FLEAS 89

In the Alps the host of C. vagabunda is the alpine chough {Pyrrhocorax
graculus) and one may hazard the guess that choughs were once its true
hosts all over the Palaearctic region which they then occupied. When
the ice began to retreat the choughs, which were adapted to the cold
conditions were only able to survive in the extreme north or in the
mountains where the climate suited them, and where they escaped the
intense competition from certain other species better adapted to the
warmer conditions. Our chough [Pyrrhocorax pyrrhocorax) which is not
confined to mountains has managed to survive precariously in a few
areas in Britain on remote cliffs. Its fleas are not known. The bird
possibly responsible for the present decline of the chough is the jackdaw
with which it comes into direct competition. This is the bird most
likely to prove a suitable host for a chough flea and it is interesting to
find C. vagabunda parasitising the jackdaw in Britain, even far inland.
The number of records of this flea from all birds in the British Isles is
twenty-four, no less than five of which are from the jackdaw. The next
largest number of records from one host is from the herring-gull (4) and
shag (4). It is possible that this boreal species of flea will once again
spread gradually all over the Palaearctic region, having firmly estab-
Ushed itself on the chough's successor.

Origins and Evolution of British Bird Fleas

There are approximately one thousand different species of mammal
fleas known in the world to-day, but there are only between fifty and
sixty bird fleas. It is thought that the bird fleas have been derived
from the mammal fleas, in relatively recent times. This can be

Map I . Distribution of the three commonest fleas from the house-martin in Britain.
• : Ceratophyllus hirundinis ; -\- : C.farreni; A : C. rustictis

Map 2. Distribution of the duck flea, C. garei, and boreal flea, C. borealisy in Britain.

• : C. garei ; © : C. borealis

Map 3. Distribution of the hen flea, C. gallinae, in Britain. (The concentrations of

records denote the chief collecting areas of five well-known collectors, Rothschild,

Waterston, Newstead, O'Mahony and Britten.)

Map 4. Distribution of the moorhen flea, Dasypsyllus gallinulae, and the shearwater

flea, OrmthopsyUa laetitiae, in Britain.
• : -D. gallinulae \ >J<: 0. laetitiae

go FLEAS, FLUKES AND CUCKOOS

deduced from the following facts. Only a small number of species of
fleas are involved and these are widely scattered throughout the
families comprising the order as a whole. Host-specificity is less
marked than in the mammal fleas, and there are relatively few cases in
which geographical variation or the formation of subspecies has
occurred. There is also a lack of specialisation in the fleas themselves.
By this it is meant that bird fleas as a whole have not, from the struc-
tural point of view at any rate, diverged very far from the mammal
fleas from which they are derived. In all cases except the genera
Dasypsyllus and Mioctenopsylla one can point with confidence to the group
of mammal fleas from which they originated. This is one reason why
bird fleas are exceptionally interesting objects of study. The change
over from mammals to birds seems a difl^icult one and few species have
been able to take advantage of this large mass of potential hosts. There
are certain conditions which appear particularly important if success
is to be achieved in this direction. Out of the 55 or so bird fleas described
27 are from birds which return to the same nesting sites year after year,
19 are from ground- or hole-nesting birds, 9 are known only from
islands, and of the remaining species a large proportion parasitise
birds which use mud in the construction of their nests. A combination
of the first three conditions is of course the most favourable. The
opportunity for straggling from a mammal to a bird host, occurs more
frequently on the ground (Plate XXXIVa) and the conditions in these
nests are more suitable for the development of the larvae. Colonies of
sea birds return year after year to the same site and thus give any fleas
which may have succeeded in living on them for one season another
chance, and again another chance, to consolidate their position and
multiply. Islands — particularly oceanic islands — afford the degree of
isolation which favours species formation. Thus we find that a rabbit
flea has succeeded in establishing itself twice on sea birds, once on
puffins and shearwaters on the rocky islands off* the west coast of
Britain (Plate XI and Map 4), and again on the other side of the
world on an auklet {Ptychorhamphus aleuticus) on Goronados Isle, Gulf of
Galifornia. On the mainland of Britain shelduck, for example, nest in
burrows, and are frequently attacked by hungry rabbit fleas which may
even be found attached to their heads, yet no shelduck flea has been
evolved. The factor which is missing is almost certainly prolonged
isolation in a relatively restricted area. On the Ganary and Pityuse
Isles a shearwater has acquired a flea of the genus Xenopsylla — the most

FLEAS 91

prevalent group of fleas on rats and mice on the mainland of North
Africa. Similarly penguins and certain other sea birds nesting on the
islands off South America, South Africa and Australia and on various
islands in between such as Bird Island, the Falkland Isles, Kidney Isle
and so forth, are infested with a genus of fleas clearly descended from
South American rodent fleas. Originally they must have picked up
these fleas in the Cape Horn area and carried them westwards and
eastwards to their various breeding stations. On the Kerguelen Isles,
in South Georgia and on Antipodes Isle, the diving petrel {Pelecanoides
urinatrix), a gull {Larus dominicanus) and a burrow-nesting parrakeet
[Plaiycercus unicolor) have each acquired a flea of the family Pygiop-
syllidae, a group of primitive marsupial fleas which are the dominant
Aphaniptera of the Australian region.

In Britain we have 16 species of bird fleas. Of these no less than 1 1
belong to the genus Ceratophyllus, The family in which these fleas are
placed contains the majority of species from the north temperate
climates of the world, and the genus in question claims 45 out of some
55 bird fleas known. These fleas have made the change over to birds
along a slightly different evolutionary path from those mentioned
above. They are clearly descended from the fleas of tree-climbing
rodents such as squirrels and certain rats (Plate Xld), and have
probably been evolved from this source twice or even more often. Both
types of hosts have developed arboreal habits, and the fleas from
squirrels are in a sense pre-adapted to the dry aerial environment of
birds' nests. The mutual arboreal habit now ensures the necessary
opportunity for straggling. Ceratophyllus gallinae has been recorded
frequently from squirrels' dreys and the squirrel flea [Monopsyllus
sciurorum) is repeatedly found in birds' nests. It has been collected from
crows' nests in Northamptonshire in localities where the rightful host,
the red squirrel, is no longer to be found.

There are two other genera of bird fleas represented in Britain
which, although they may be included in the same family, are not
closely related to Ceratophyllus. The first is Dasypsyllus gallinulae, a flea
found on a wide variety of birds nesting on or near the ground. This is
rather an ancient and obscure genus and it is only possible to hazard
a guess as to the mammal fleas from which it is derived. The arrange-
ment of bristles on the head is somewhat similar to that found on a
prevalent genus of South American fleas, Pleochaetis, which may have
given rise to Dasypsyllus. All the other known species, except one, are

g2 FLEAS, FLUKES AND CUCKOOS

found in South America on birds such as the cheu-can {Pteroptochus
rubecula) and it is a group which certainly originated in the Neotropical
Region. D. gallinulae is also found in British Columbia (North America)
where it has developed into a distinct sub-species. Possibly this is the
route by which Europe received this single representative of the South
American fauna. The other genus is represented by one of the most
interesting fleas in Britain, Orneacus rothschildi, of which nine specimens
only are known*. These were taken from a house-martin's nest situated
on the cUffs at Kinneff on the east coast of Scotland. A shghtly different
subspecies of the same flea was collected in the Swiss Alps by Jordan
and Rothschild. The other known species of this genus was found in a
martin's nest in Ladakh, Kashmir at 10,500 feet. These fleas are derived
from quite another group of mammal fleas, the genus Citellophilus,
parasitising ground squirrels (Citellus), and with these they show a
striking affinity. It is difficult to guess the place whence the Scottish
martins got these fleas. The fossil record proves that the mammal
Citellus was present in Britain (Thames Valley) in the Pleistocene many
thousands of years ago. The nearest species of Citellophilus to-day,
however, is found in the Pyrenees. It is probable that the switch-over
from ground squirrels to house-martins took place somewhere in the
Palaearctic region, but the possibility cannot be ruled out that Orneacus
was brought to east Scotland by migrating martins which had picked
up the fleas on their travels.

The common house-martin flea {Ceratophyllus hirundinis) as we have
seen has a very wide distribution and is also found on the martins
breeding in Kashmir.

It has already been mentioned that among British bird fleas there is
one representative of the family PuHcidae (to which the human flea
Pulex irritans belongs) . This is the shearwater flea, Ornithopsylla laetitiae,
descended from one of the rabbit fleas of North America. In the Palae-
arctic region there is only one species of rabbit flea of this family found on
the common rabbit and one (Hoplopsyllus glacialis) on the arctic hare
but in North America there are at least ten species and sub-species.
Puffins and rabbits Hve in close proximity — even using each other's
nesting burrows — on the rocky islands off the coast of Britain. In
fact our rabbit flea has been taken off the puffin on Skomer Isle.
The first idea that occurs is that the common rabbit flea at some
remote period passed on to the puffins and shearwaters, and gradually
♦Since re-discovered in Aberdeenshire (Allan 1950).

FLEAS 93

became modified into Ornithopsylla laetitiae. It would thus repre-
sent its direct ancestor. A detailed study of the morphology of
these fleas, however, shows that this is extremely unlikely and the
attractive theory has to be abandoned. Both, no doubt, originated from
North American rabbit flea stock [Hoplopsyllus) ^ but are not themselves
very closely related. Curiously enough little or no collecting has been
done from nests of sea birds on the eastern coast of North America but
it is highly probable that some of these, too, harbour species descended
from rabbit fleas. If and when such fleas turn up, they may give
us a more direct clue to the immediate ancestry of Ornithopsylla
laetitiae.

Along with the house-sparrow, the common hen flea of Europe was
also introduced into the United States, where it has spread on to
numerous wild birds as well as domestic poultry. Up to date there is no
parallel case of a modern introduction of a bird flea from North
America into Europe, but occasionally a rather weird flea, the South
American parrot stick-tight flea, is taken ofif a variety of captive birds
at the Zoo including tame pigeons. There is always a possibility that
this species might spread to native birds via the ubiquitous sparrow
which hops in and out of the aviaries at the Zoo. In South America it
has a wide range of hosts, but was first recorded from a parrot. This flea
is a relative of the jigger ( Tunga penetrans) which burrows beneath the
skin and heavily infests the feet of the natives in South America and
Africa. It causes great irritation and abscesses develop at the spot
where it is embedded as the result of secondary infections. Like the
jigger the female of the parrot stick- tight flea is permanently fixed to the
host but it remains attached to the surface of the skin. The modifications
arising from the sedentary habit (see p. 63) can be studied in this and
allied species of fleas.

It has already been pointed out (p. 68) that bird fleas — at least
C. gallinae — can breed on mammals as well as on their true host. A
relatively loose bond with the host was probably one of the character-
istics necessary to allow the change from mammal to bird to occur in
the first place. Consequently bird fleas are frequently found on mam-
mals. When a cat catches a sparrow for example, it generally carries
it about for a while and allows it to get cool. The fleas soon leave
the bird, and at times change on to the cat and so in a small way
avenge the death of their host. How long they survive and whether,
outside the laboratory, they do in fact breed on a mammahan host is

94 FLEAS, FLUKES AND CUCKOOS

not known. Such species as the sparrow flea and the hen flea have been
taken off cats and many other predatory animals such as rats,
stoats, weasels, and foxes. Conversely certain mammal fleas are not
infrequently found as stragglers on birds of prey, especially owls (Plate
VI), or on small birds which to a certain extent share their habitat.
Thus the rabbit flea straggles on to burrow- and ground-nesting birds,
and has been taken off ducks, puffins, shearwaters and partridges. The
American and British squirrel fleas are found in a variety of arboreal
nests, and occasionally on the bodies of birds themselves. Bat fleas have
been found on the swift, the human flea on wild duck, and the hen flea
and house-sparrow flea on man himself.

It is not difficult to imagine new species arising in this way, providing
some accident supplies the necessary isolation. On Skomer Isle one can
conceive our rabbit flea establishing itself permanently on the shear-
waters, and thus giving rise to a situation which may puzzle and confuse
future systematists.

Even among such closely related species as our eleven Ceratophyllus
we can trace certain evolutionary trends and try to construct a phylo-
genetic "tree" by studying details of morphology. For example by
grouping them according to the degree of thickening and hardening
(sclerotisation) of certain internal organs of the female, and the shape
of the receptaculum seminis (Plates XIII and XIV) we find they fall
into two main groups. The first contains the three British species
C. garei, C. borealis and C. columbae from the British fauna and one
species from Turkestan and another from North America. This group
shows the least sclerotisation and has a kidney shaped body to the
receptaculum. It is descended from the Monopsyllus sciurorum group of
squirrel fleas (Plate XIIIc). The second group, which falls into two
distinct sub-groups, shows sclerotisation and a progressively more
vermiform body to the receptaculum. These fleas represent a second
evolution from the same genus of rodent fleas, this time from the Mono-
psyllus anisus group (Plate XI Vg), which are found on rats and squirrels
in the Pacific area of the Palaearctic region. Our bird fleas may have
originated from that area via North America. The first of these sub-
groups contains C. hirundinis and C. rusticus from our fauna. The
second sub-group, with the most pronounced sclerotisation, includes
all our other Ceratophyllid bird fleas and many foreign species,
and incidentally all those which have become adapted to relatively
dry nests.

FLEAS 95

In considering the evolution of a genus like these bird fleas which
appear to have been derived at least twice from closely related mammal
fleas — possibly at different times and in widely separated parts of the
world, it must not be forgotten that certain characters from an ancestral
flea may also re-appear in different branches of one stem.

One very interesting Ceratophyllus must be mentioned here. Although
it has not yet turned up in Britain it seems to us there is quite a
good chance that it will eventually be discovered on the stoat and
marten in Northern Scotland. This is C. lunatus, a former bird flea
recorded from the Alps, Alaska, North Sweden and Northern Russia,
which has once again reverted to a life on mammal hosts. This return
to its original type of host must have happened before or during the last
Ice Age, judging from the famihar boreal-alpine distribution (see
p. 87) of the flea. It also must have occurred fairly early in its history
as a bird flea, for although it displays certain features typical of bird
CeratophyUi the modifications of thereceptaculum seminis usually assoc-
iated with an avian host have been arrested at a relatively early stage.

The fact that there are several bird fleas with the boreal-alpine
type of distribution proves that they had already changed on to avian
hosts at any rate before the end of the last Ice Age in Europe.

The Effect upon the Flea of a Change
TO A Bird Host

It has been pointed out (p. 90) that the change over to bird from
mammal host must have taken place in relatively recent times. Never-
theless, this new environment which involves such great differences in
food, temperature and habitat, has already left its mark upon the fleas.

A study of the Ceratophylhdae and the PuHcidae shows that the
trends of evolution are different within the two main famihes or super-
families. When a switch over to a bird host occurs it seems to speed up
these family trends.

In the GeratophylHdae there are four genera of bird fleas, Cerato-
phyllus, OrneacuSj Dasypsyllus and Mioctenopsylla, and two species from
the genus Frontopsylla* (chough fleas) which have unquestionably been
evolved from different groups of mammal fleas (p. 91). Nevertheless,

♦Since the completion of this manuscript Frontopsylla laetus has been found by
Allan (1950) in a house-martin's nest in Kincardineshire, Scotland.

g6 FLEAS, FLUKES AND CUCKOOS

despite their varied origins they all show a marked increase in the
number of teeth in the pronotal comb (see Plate X). The mammal
CeratophyUi in question rarely have more than 22 teeth in these
combs, but the bird fleas all have from 26 to 40. Thus in all bird
Ceratophyllidae we find without exception a combination of two
facts (a) the environment "bird" (b) a larger number of spines in
the pronotol comb. This structural modification, therefore, appears to
be connected with, or possibly is the direct consequence of the change of
host, and thus presents an example of convergent evolution.

In the family Pulicidae there is a general tendency towards a
reduction and final loss of combs. The change to bird host has apparent-
ly accelerated the process. This phenomenon can be observed in the
two genera of bird fleas derived from rabbit fleas (Spilopsyllinae). The
rabbit fleas (Plate X) still possess pronotal and genal combs or at
least a pronotal comb, but the shearwater and auklet fleas have neither
one nor the otlier (Plate XI).

Thus the change of hosts has produced convergent evolution in
both famflies, but leading in opposite directions. When a CeratophylUd
flea leaves a mammal and becomes permanently parasitic on birds the
result is additional teeth in the pronotal comb, but if a PuUcid flea
takes this same step, the reverse appears to happen and one must expect
an increased rate of reduction and final loss of the combs. Therefore,
when studying this type of evolution it must always be remembered that
the eflfect of the change depends on the derivation and nature of the
flea, as well as on the nature of the host and other environmental factors.

There is another morphological modification which can be observed
in certain bird fleas, which is almost certainly associated with the change
of host. This is a tendency towards a shift in position and ultimate
reduction of the plantar bristles of the feet. The normal number of
plantar bristles is five and this primitive condition is stiU found in the
Ceratophyllidae. In the whole family PuHcidae there is a tendency
towards reduction, and all the rabbit fleas for example, have only
four pairs. Once again the condition is accentuated in the bird fleas,
for both in the two species derived from rabbit fleas and the two
derived from the tropical rat fleas, this reduction has developed
farther than in any other allied fleas. The third pair of plantar bristles
shows either a change of position — a shift upwards and inwards
which Jordan describes as "crowding towards the apex" — or is lost
altogether.

FLEAS 97

Despite the fact that this trend is not present in the family Cerato-
phyllidae as a whole, the kittiwake flea (Mioctenopsylla arctica) also
shows a weakening and loss of tarsal bristles — at least in the hind
tarsus. In this case the mysterious influence which produces these
parallel changes in bird fleas seems to affect certain species of the whole
order irrespective of family trends.

It has already been seen (p. 42) that among parasites there is
often a tendency towards loss of eyes, and this is particularly marked in
animals which live in the host's nest. In the case of fleas, however, the
matter is by no means so simple. It is true that many nest dwelhng
species are blind but the bird fleas, which are nest dwellers par
excellence, all have well developed eyes. There appears to be some
connection between the life of the host and the degree of development
of the flea's eyes. Thus broadly speaking nocturnal animals — for
example bats — are parasitised by bhnd fleas and diurnal animals by
fleas with eyes. It is remarkable nevertheless that all bird fleas, even
the sand-martin and shearwater fleas which live in nests in burrows,
should have retained their eyesight. The question is a comphcated one
and further research into the problem would be of great interest.

The changes referred to above are morphological ones and therefore
relatively easy to detect. There must be many other changes hnked with
a parasitic life on birds, physiological ones for example, about which
httle or nothing is known. One such adaptation has already been
mentioned, namely the development of a well defined breeding season
in C. gallinae to coincide with that of the host. It is most probable
that this feature is common to all the bird fleas of the temperate
zones.

From time to time isolated observations are made on bird fleas
which may bear some relation to their particular mode of life. As we
have noted, one of the most vital problems which annually confronts
the majority of bird fleas is the question of survival when the nest is
deserted at the end of the breeding season. In this situation widespread
scattering is an advantage. It is, therefore, not surprising that C. gallinae
and C. garei are so frequently collected far removed from either host or
nest (p. 81). This ability to hibernate or rest, fasting, under the bark
of trees, among leaves, in cracks on fences or in piles of rubbish, there to
wait for a passing host, seems especially well developed in bird fleas.
As we have already suggested, the need for wide dissemination may
also account for the mass migration of certain species. One of the

g8 FLEAS, FLUKES AND CUCKOOS

mammal fleas which has been noted in Russia for these periodical mass
movements is closely related to the bird Geratophyllids. In this case
most of the fleas move out of the burrows at night, but on several
occasions Waterson in Scotland witnessed large swarms of hungry fleas
leaving birds' nests in broad dayhght. They bit viciously at him when
they landed on his outstretched arm. Possibly climatic changes or hunger
initiate the exodus. In Finland one observer noted that the common
hen flea migrates from open nests if the temperature falls below i4°C.
However, little or no research has been done in this field, so we can
only speculate.

As we have explained (p. 136) the Mallophaga have evolved
the habit of "hitch-hiking" or phoresy, as it is called technically, as a
means of reaching another host when their own dies; there are at least
two records of them attaching themselves to fleas ! However, fleas, with
their highly developed powers of leaping do not apparently make use of
winged flies for transport. A few moments after the bird dies they come
to the surface of the feathers and jump off into the blue. There is one
known case, however, when a bird flea was found on a queen wasp and
another in a wasp's nest. Wasps being carnivorous may have picked up
the fleas when visiting corpses. This type of relationship often escapes
notice and although these two occurrences are probably accidental, it is
well worth looking out for further evidence of association between bird
fleas and wasps.

Effect of Fleas on their Bird Hosts

Mammal fleas are notorious carriers of disease. As vectors of
bubonic plague they have been directly responsible for the deaths of
millions of rats and miUions of men. A large number of less well known
diseases are also spread by them. Thus they carry a roundworm
{Filaria) which eats out the hearts of dogs, besides several of the common
tapeworms, for which they serve as intermediate host. They spread at
least two serious diseases among rabbits and hares, one of which,
tularemia, can also affect other animals including man. They act as the
intermediate host for a species of trypanosome (T. lewisi) parasitic
in rats and another in rabbits, and they can also become infective for
endemic typhus. Salmonella and possibly leprosy. So far, however, they
are not known to be vectors of any serious disease of birds although bird

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Plate XVIII

c. Pupa within cocoon ( x 37)
LIFE-CYCLE OF FLEA

J. G. Bradbury

FLEAS 99

fleas can transmit the trypanosomes referred to above. Their harm-
lessness in this respect may be more apparent than real, due to the fact
that we are ignorant of the true role they play. However, fleas have
only been closely associated with birds for a relatively short period, and
therefore they may not have had time to become adapted as carriers or
intermediate hosts of other bird parasites.

Occasionally plague-carrying mammal fleas straggle on to birds.
Thus, in the Rothschild collection there is a specimen of the tropical
rat flea taken off a bird. Certainly the hen stick- tight flea, which is also
frequently a parasite of rodents, can carry plague from wild to domestic
rats. Birds, when they nest or roost in rat-infested houses or chicken
coops must be regarded as potential reservoirs of plague. On the other
hand the Ceratophyllidae, which are the commonest and largest group
of bird fleas, are not very effective vectors of plague.

In the case of the hen stick- tight flea, which is not a British species, the
direct effect of an infection is very serious. Poultry lose weight, egg laying
is reduced, and birds not infrequently succumb to heavy infestations.

The effect of a bite on a human being, in the case of non-sedentary
species of fleas, varies considerably from one individual to another. The
local swelling which causes a certain amount of irritation is probably
due to the enzyme which entered the wound in the insect's saliva. As
time goes on, a certain immunity is usually developed and elderly
people hardly react at all to a flea's bite. Whether this is also the case
in birds is not known.

In any case it is extremely difficult to gauge the direct effect of fleas
on nestlings. The few specimens living on the bodies of adult birds can
be of little or no importance but several thousand fleas in a nest full of
young birds must present a serious menace. The mortality from all
causes among nestlings is high, sometimes sixty-five per cent, of all
those hatched in the case of small passerines. It seems reasonable to
suppose that when a single population of fleas runs into four figures the
constant drain of blood must be a contributing cause of death among
the more delicate young birds.

Bird Fleas and the Evolution of Birds

In the Mallophaga as we have seen, these parasites have in many
cases evolved at a somewhat slower rate than their hosts. The bird's

FFC H

100 FLEAS, FLUKES AND CUCKOOS

body has provided the feather hce with a more or less constant environ-
ment and one which has altered them less than the impact with the
outside world has altered the host itself. Therefore, the relationships of
the parasites often throw light on the relationships of the birds.

In mammal fleas, although they are altogether much less closely
bound to their hosts than feather lice, and in the larval stages also have
to cope with climatic and other outside influences, the same type of
phenomenon can be observed. For example the extraordinary and
unique group of fleas known as the helmet fleas of Australian marsupials
are also found on the pouched mammals of South America, thus once
again confirming the latter's true relationship with the Austrahan
marsupials and demonstrating their common origins.

The situation in the case of the bird fleas is, however, very different.
The change over to birds is altogether too recent to provide evidence of
host relationship. What these fleas often provide, however, is a clue to
the past geographical history of the bird. For example the European
chough fleas [Frontopsylla frontalis and F, laetus"^) which may still be added
to the British list are descended from a genus of the Amphipsyllidae, a
family of fleas from Central Asia and China. The choughs are con-
sidered by many ornithologists to be a strictly Asiatic group which has
extended its range into Europe some time during the Pleistocene, so
the presence of these fleas supports their theory. The penguins breeding
in the Australian and South African areas have fleas clearly of South
American origins and this indicates from which area these birds
extended their range eastwards. Other examples of this type could be
given, but sad to say here again no definite conclusions can be drawn
from the British fauna, because not enough is known about the fleas
of our own birds. It is amazing how little collecting of bird fleas has
been done by British ornithologists, especially if one considers the
attention now given to almost every aspect and detail of bird fife.

Host Specificity and Host Preference

Among bird fleas there are three main types of host preference.
The first and most obvious is when a species of flea is adapted to one
species of bird only — in other words it displays strict host specificity.
In an ancient group of bird parasites like the Mallophaga, where louse

*Since discovered in Aberdeenshire (Allan 1950) in the nest of the house-martin.

FLEAS lOI

and bird have evolved through the ages together, this is the rule rather
than the exception. Fleas having, on the other hand, only relatively
recently moved on to birds, there has not yet been time for many such
close relationships to develop. An example of strict host specificity in
the British fauna is provided by C. rossittensis, which has never been
recorded except on the crow {Corvus corone), either in this country or on
the continent. The rock-dove flea, the sand-martin flea and the four
house-martin fleas can also be considered host-specific although a
limited amount of straggling occurs.

The second type of host preference is illustrated by fleas which show
a more or less marked predilection for certain famihes of birds. For
example a North American flea, C. difflnis, is essentially a parasite of the
thrushes, and despite its wide variety of hosts in Britain C. garei is un-
doubtedly partial to ducks and geese. This becomes more apparent
when it is surveyed throughout its range.

Finally we have a third type consisting of a few species which
apparently show no host preferences and are equally at home on all
birds. When sufficient collecting has been done and the results properly
analysed it will be found that this indifference is more apparent than
real. No one will deny that C. gallinae, with its sixty-five diflferent
bird hosts in Britain alone, has cathoHc tastes, but the statement so
frequently met with in print that it is "common on all birds" is equally
false. The hen flea has not, for example, been recorded off* ducks and
geese (order Anseriformes) or from plovers and waders (order Chara-
driiformes) .

In the chapter on distribution it has been mentioned that the three
commonest bird fleas in Britain can be "zoned" according to the type
of nesting site which they favour. Despite the considerable overlap
which occurs it is true to say that the highest proportion of C. gallinae
infestations are found in nests in tree tops or elevated situations (dry
aerial nests), the highest proportion of D. gallinulae in nests in lowly
situations such as brambles, walls and small bushes (damp nests), and
the highest proportion of C. garei infestations in ground nests and
in swampy situations (wet nests).

At times host preference and nesting site preference must cut
across one another. A nest may be all that the larvae require but the
host prove unattractive to the adult — or vice versa. For example the
nesting habits of the pheasant and partridge are to all appearances
remarkably similar and in fact these birds not infrequently use each

102 FLEAS, FLUKES AND CUCKOOS

Other's nests, which seem in every way equally suitable to fleas. All the
three common species referred to above have been found in the nest of
the pheasant but so far the only flea recorded from the partridge is
C. garei. It would appear that in some way the partridge is unattractive
to C. gallinae and D. gallinulae^ a fact which overrides the suitability of
the nesting site.

The swan is a bird from which no fleas whatsoever, even stragglers,
have been recorded, despite the fact that its nest is both obvious and
accessible to collectors, and appears ideal for the requirements of C.
garei. We can do no more than guess at the reasons for its immunity.
Possibly the blood of the swan is unattractive to fleas, or its skin so
tough that the flea's mouth parts fail to pierce it, or the nest debris is in
some way unsuitable to the requirements of the larvae.

One of the facts which strikes every student of bird fleas is the rela-
tively large variety of species which parasitise martins and swallows.
No less than seventeen fleas are specific to these hosts. Out of our own
fauna of fourteen bird fleas, five are martin fleas and of the rest, all but
four have been recorded from them as stragglers. Moreover, an un-
usually high proportion of martins' nests are infested, and the flea
population within individual nests is relatively very large. It has
already been pointed out that the habits of martins are helpful to
fleas. Thus they frequently build compact mud nests, or make nests in
holes in the ground or in caves, which suit the larvae and originally
favoured successful straggling. They also associate in colonies, so that
fleas off a dead host have not far to seek another suitable victim. What
is even more important, martins tend to return year after year to the
same nesting sites. These characteristics in themselves, however, are
not sufficient to ensure either a large or a varied fauna. For example
the swifts also construct mud nests, associate in colonies and return
year after year to the same site, but they have failed to acquire a single
flea peculiar to themselves. The only species recorded from their nests
are the hen flea and sparrow flea, both of which were probably im-
ported by sparrows which frequently usurp old nests and leave behind
a few parasites. The fact is we do not know why one whole group of
birds, such as the swifts, is unattractive and another, Hke the martins,
is apparently equally attractive to fleas.

FLEAS 103

Enemies of Fleas

At all stages of its life history the flea no doubt has enemies. But
these have been imperfectly studied and it is not known how populations
of fleas are kept in check and whether their numbers are reduced by
parasites and disease.

As an adult the flea's most important enemy is undoubtedly the bird
itself. Buxton has shown (p. 80) what large proportions are eaten by
their mammalian hosts. Birds are scrupulously clean and probably their
thoroughness in preening has forced their fleas to become nest dwellers.
In other words, only fleas which are to a certain extent pre-adapted to
a life in the nest can succeed as bird fleas. However, the nidicolous
existence exposes them to dangers from other animals occupying the
same habitat. Staphylinid and Histerid beetles have been observed in
nests catching and devouring fleas by the dozen. Ants also, if they
come into contact with fleas — which most often happens in old ground
nests — devour both the adult and larval stages.

The sand-martin fleais particularly susceptible to a Gregarine (Proto-
zoan), a hyperparasite which is found in the mid-gut of larvae, pupae
and adults. Damp nesting sites favour the survival of the spores and the
reinfection of the flea, and for this reason between 65 and 100 per cent,
of the sand-martin flea population may be infested, but in the case of
C. gallinae the figure is steady at about 5 per cent. Its eflect on the
flea is not known.

The plague bacilli can often prove fatal to the fleas which transmit
them, by multiplying in their gut and thus mechanically blocking the
proventriculus, when the flea starves to death. Certain roundworms,
apart from those which use fleas as intermediate hosts, feed on their
reproductive organs and can effect complete castration.

A hymenopterous parasite, Bairamlia fuscipes, lays its tgg in the flea
larva and eventually kills it, during the course of its own development.
The only records from Britain are from squirrel and hen fleas.

By far the most famous parasites of fleas are the mites which live
in the nest and destroy their larvae and pupae. There are numbers of
different species which inhabit both bird and mammal nests, and they
originally sprang into fame when Loewenhoek, over two hundred years
ago, first described them preying upon the larvae of the pigeon flea.
This discovery inspired the hackneyed but immortal lines : " Big fleas
have little fleas upon their backs to bite 'em." Hirst found that these

104 FLEAS, FLUKES AND CUCKOOS

mites had a special affinity for the pupal case which they completely
destroyed. In the laboratory they can, in this way, eliminate whole
flea cultures.

One of the most curious and interesting facts about these mites is
that in the hypopus stage (see p. i8) they use the adult flea as a means
of transport to new nests. They attach themselves to the outside and
even creep just beneath the chitinous plates or sclerites and hang on
firmly by their sucking disks which are special adaptations for "hitch-
hiking" purposes and are developed only at this stage. In some
mysterious manner the mites can evidently distinguish between the sexes
of the fleas, for they almost always attach themselves to females — a wise
precaution for a parasite preying on the larval stages of the flea. The
mites differ considerably in size. The species found on 0. rothschildi
(Plate V b) is one of the largest parasitising British bird fleas. Those
illustrated on Plate V a, which look like ghosts beneath the sclerites of
the host, are considerably smaller. These mites have not been identified
with certainty. Sometimes as many as 150 hypopus larvae have been
found attached to a single "transport." Such numbers greatly hinder
the movements of the flea and in some cases may even cause its
death.

We have already seen that when the bird host dies and grows cold,
the fleas leave it and seek their fortunes elsewhere. Similarly, when the
flea dies the mites also leave it. They moult, shed their sucking disks
and change into octopod nymphs. How is it that the "hypopus" mites
are aware their transportation has broken down ? Perhaps the sudden
cessation of movement is the stimulus to which they respond. One of
the older writers observing them at such a moment wrote : "In
bestirring themselves from their inactive condition one would imagine
that a state of demoralization had seized them, for they were seen to
pry free the sucking disks, leave their perch and move away from the
dead host."

Classification

It is convenient to classify animals — that is to name them, describe
them accurately and then arrange them in groups — just as it is con-
venient to name and classify the goods for sale in a shop. It is reasonably
easy for a customer to locate cheese in Harrods' stores, because food, as

FLEAS 105

a commodity, is sold in one part of the building, and certain types of
food, such as meat, fish, and groceries, are conveniently assembled at
different counters. The commodities in Harrods' stores are, broadly
speaking, classified according to their function in the world of men. That
is to say goods intended for wearing, eating, drinking, reading or
smoking are sold in different departments. This makes shopping
easier than if they were, for example, classified according to their colour,
when you would find fire engines, tomatoes, " Who's Who," seahng
wax and flannel petticoats all in the same department.

Animals are classified scientifically with two main objects in view.
Firstly, to render the animals in question easy to deal with from a
purely practical point of view — to identify them quickly and accurately,
to be able to describe them in print clearly, and to read about them with
understanding. Secondly, to demonstrate their biological position
among all hving things. In other words they are classified according to
the degree of fundamental relationship which exists between them.

To the layman it is obvious that a cat and a leopard are more alike
than a cat and a canary. On the other hand they might well be de-
ceived by a whale's superficial and outward resemblance to a
shark, and be excused for thinking that both these animals are
fish. Similarly a man from Mars might decide after a glance at
a Dutch cheese, that its rightful place in Harrods' stores was the toy
department and not the grocery counter.

Classification should serve as an aid to study, but man's passion for
pigeon-holing knowledge frequently results in the creation of a hopeless
muddle. " The human understanding, from its pecuhar nature,"
remarked Francis Bacon, "easily supposes a greater degree of order
and equaHty in things than it really finds." Animals cannot be
forced into a fixed scheme, and however profound the biological truths
reflected in such classification, all workable and practical schemes of
this sort are to a certain extent arbitrary and therefore unsatisfactory.

When a classification is being built up all the characteristics of the
animals concerned have to be taken into consideration, ranging from
morphology and life history to differences in behaviour and habits.
In practice, however, there are some characters which vary more than
others, some which prove more reliable and more stable, and again
others which are more easily seen under the microscope or which lend
themselves to relatively brief and simple description. Thus, for example,
the bones and teeth are largely used as a basis for dividing up the

I06 FLEAS, FLUKES AND CUCKOOS

mammals into families and genera, whereas the exoskeleton or hard outer-
covering, is used in the case of fleas.

It is not easy to describe the simplest object in precise language.
The layman complains bitterly about the obscure wording of legal
documents, emergency regulations and scientific papers. Yet anyone
who has tried his hand at describing a piece of Hnoleum or a gate-
legged table in such a way that it cannot be mistaken for any other type
of floor covering or table, will appreciate some of the difficulties in-
volved. A trained lawyer is required to draw up a legal document
and a trained biologist to classify an insect correctly and ade-
quately.

Although unavoidable, the use of this technical jargon is, at first,
rather irritating and confusing to those who are unfamihar with
scientific descriptions. This fact, and also the obscure nature of some of
the characters used in separating one species from another, makes
systematics and classification seem fantastically dull to the average lay-
man. Sooner or later even the professional zoologist reflects gloomily
that all roads lead to the counting tray or to the measurement of combs
and beaks. Nevertheless this detailed and rather tedious work is
absolutely essential. Commenting upon the fact that the spread of
epizootic plague is governed by the flea-species factor Hirst remarked :
" The discovery is but further testimony to the essential unity of science
in its bearings on the welfare of the human race, for it is the natural
outcome of the purely zoological researches of Rothschild and Jordan
on the systematics of the Siphonaptera." In fact sound systematics are
the foundations upon which all biological theories, great or small, are
built. Disgruntled zoologists should reflect that Darwin's first important
pubhcation was a treatise on the systematics of barnacles.

Fleas are insects, and share with all other insects certain character-
istics of their Class. Within this huge assembly they form a rather
isolated Order. They are descended from winged ancestors — a fact
which can be inferred from their structure and the study of analogous
cases — but the various intermediate types have become extinct and
there are no living insects which show the transitional stages or even
suggest what they were like.

When the fleas themselves are divided up they fall into two fairly
well defined superfamiUes, and here again we can do Httle more than
guess at the characters shared by the common ancestors of these two
large groups. The superfamiUes, famihes, genera and species,which

FLEAS 107

each represent more and more restricted categories, are distinguished
by such characters as the form of the sclerites and their internal
supporting rods, the presence or absence of certain combs or spines, the
shape and structure of the genitaHa and so on.

As we move down the scale and reach closely related species,
minute differences have to be taken into consideration. These
differences may seem trivial and even unimportant to the unpractised
eye, but they have been selected after a comparison of all known fleas.
They are the characters which specialists have found from experience
can be rehed upon, and which reflect the natural relationship of the
order as a whole.

In written scientific descriptions no detailed account of the animal
in question, or group of animals, is given — only the essential points are
described. For practical purposes such descriptions must be as brief as
possible.

The two superfamiHes into which the fleas are divided can be
characterised as follows : —

L Superfamily Ceratophylloidea. (Plate XVII). This is a large
superfamily with the following morphological characters : A sword-
like ridge running down the inside of the outer wall of the mid-coxa.
A pointed tooth present at the apex of the outside of the hind tibia.
Abdominal terga II — VII with more than one row of bristles. Pygidium
with more than sixteen pits on each side.

This superfamily includes the Ceratophyllidae which contain
thirteen out of our fourteen bird fleas.

11. Superfamily PuHcoidea. (Plate XI). No swordlike ridge
running down the inside of the outer wall of the mid-coxa. No
pointed apical tooth present at the apex of the outside of the hind
tibia. Abdominal terga II — VII with at most only onerow of bristles.
Pygidium with fourteen or fewer pits each side (Plate XIX).

This superfamily includes the family Pulicidae which contains the
most notorious of all fleas, the tropical rat flea {Xenopsylla cheopis), the
vector, par excellence, of bubonic plague, and the human flea {Pulex
irritans). The only representatives among the British bird fleas are the
shearwater flea {Ornithopsylla laetitae) and Hen Sticktight flea (see p. xiii).

Although the characters separating these two families appear rather
obscure, they present in practice quite a striking contrast. The Puhcidae

I08 FLEAS, FLUKES AND CUCKOOS

are small, compact, and rather dumpy, whereas the Ceratophyllidac are
elongated, loosely built fleas.

All the characters mentioned here, besides of course many others,
can be picked out on the labelled photograph.

The British Bird Fleas*

THE COMMON HOUSE-MARTIN FLEA, Ceratophyllus hiruudinis; farren's
HOUSE-MARTIN FLEA, C. farreui; the scarce house-martin flea,
C. rusticus; the Scottish house-martin flea, Orneacus rothschildi (Plates
XIII-XVII and Map i). All the first three species are found pullu-
lating in the nests of house-martins. The fourth, the Scottish house-
martin flea, is very rare and has only been found once — in Scotland.
Nine specimens were revealed among 4,000 C. farreni, thus showing
that it is well worth while examining all the fleas present in a single
nest.

The first reference to a British bird flea concerns one of these species.
Hill (1752) remarked that "fleas are not confined to man and quad-
rupeds but are also found in swallows' nests." However, he shared
Linnaeus' view that they were all one species. Long after it was known
that mammals harbour different sorts of fleas, it was still thought that
all bird fleas were one and the same " Pulex avium", until Dale's
unfortunate decision to name every flea from a new bird host
as a diflerent species greatly increased the confusion.

C. hirundinis is described as the commonest and most widespread of
the British house-martin fleas, C.farreni as a fairly common species, and
C. rusticus as rare. The two former species have both been recorded in
several thousands from single nests, but until quite recently (see
below) C. rusticus has only been found in small numbers. The ecology
of these fleas is extremely interesting but the study of it has so far been
entirely neglected. All three species have been found in the same nest,
in the same locality, in the same season and apparently all occupy the
same ecological niche. They would, therefore, appear to come into
direct competition with one another. This is of course^a most unlikely

♦Since the completion of this manuscript Allan (1950) has found a further species
in the nest of the house-martin in Scotland, Frontopsylla laetus, a bird flea with an
alpine-boreal type of distribution. He also collected a further series of Orneacus
rothschildi from the same nest.

FLEAS 109

State of affairs and it remains to be seen what are the limiting factors
within the nest for each species.

The total records of these house-martin fleas, collected from all
known sources, in Great Britain and Ireland are as follows : —

C. hirundinis Cfarreni C, rusticus 0 . rothschildi

61 records 43 records 33 records i record

It seems likely that C. rusticus is on the increase in this country. Up to
1923 it had only been recorded six times and was absent from both
Tring and Ashton. In 1935, Rothschild examined sixteen nests from
these two localities and it was present in them all. The three species
were represented as follows : —

C. hirundinis Cfarreni C. rusticus

722 74 353

(present in 15 out (present in 11 out (present in 16 out

of 16 nests) of 16 nests) of 16 nests)

It is a well known fact that in recent years a few British butterflies, such
as the comma and white admiral, have increased their range and
changed their status from "rare" to "common." Similar fluctuations
may easily occur among the Aphaniptera.

The vast numbers of these fleas in single nests raise the question
as to what factors limit the size of a population. At present it is a
complete mystery why a house-martin's nest should regularly harbour
hundreds, if not thousands, of fleas and other birds' nests, apparently
equally suitable, a mere dozen or so.

The distribution of these fleas outside Britain and their origins are
dealt with on pages 85 and 94.

The sternites of the males and receptaculum seminis of the females
are figured on Plates XIII-XVI. The vermiform shape of the body
of the receptaculum of C. hirundinis, C. farreni and C. rusticus should be
compared with the barrel-shaped organ of 0. rothschildi. The contrast
is striking (see pp. 92-95).

It is worth noting that the first specimen of C. rusticus described in
this country was a straggler off a wood-pigeon. It is one of our smallest
bird fleas, generally measuring less than 2 mm. in length.

no FLEAS, FLUKES AND CUCKOOS

THE ROCK-DOVE FLEA, Ceratophyllus columbae (Plates XIII, XV,
XVIIIc). Life in caves brings the various occupants into faidy close
proximity and favours the exchange of parasites. It also provides a
certain degree of isolation from the outside world. It is, therefore, not
surprising that our rock and cave dwelling pigeon [Columba livid)
should be the one pigeon to harbour a specific flea parasite. In the past
there has been much controversy concerning the origins of the domestic
bird, although it is now generally agreed that it is the same species as the
rock-dove. The presence of C. columbae on the wild rock-dove and on
our domestic pigeon is another piece of evidence in support of this
theory. C. columbae has never been recorded in Britain from the stock-
dove and only once from the wood-pigeon, and this was in London
where it can be regarded as a straggler from a tame pigeon. It also
occasionally wanders on to sea birds which nest on rocky cliffs.

C. columbae is a particularly easy species to identify, especially in the
male sex, which has a characteristic bundle of bristles right at the end
of the eighth sternite. Its absence from the dove cotes of the United
States has been noted by Jordan.

THE DUCK FLEA, C. garei, and the boreal flea, C. borealis (Plates
XII, XV, and Map 2; see also p. xiii). These two fleas, which
are almost black to the naked eye, are so alike that only a
specialist can be expected to tell them apart. Both are primarily
parasites of ground-nesting birds, and C. garei is the only British flea
which can tolerate the conditions found in ducks' nests. It is recorded
from the eider duck, pintail, shoveler, red-breasted merganser and so
on, hosts from which no other British bird flea has been taken. Never-
theless, it is at home in a really large range of nests, and in Britain alone,
is recorded from 48 different species of birds, including such widely
different hosts as the corn-crake, bearded tit, redshank, wryneck, artic
skua, long-eared owl and goldfinch.

Its range extends from the Shetlands south to Cornwall and it is
also recorded from Ireland (Map 2).

C. borealis has a much more restricted habitat and is found in Britain
only in the outlying Western Islands and Orkney (see p. 87). In this
country it appears to have a slight preference for the wheatear and
has also been collected from the same host on the Island of Ushant
during the birds' return passage from Africa. The only flea known
from the cuckoo is C borealis also taken from a specimen in Ushant.

FLEAS III

The bird may have picked it up from the nest of its fosterparents
(Plate XXXVIIIb) or during migration along the same route as
wheatears, pipits or wagtails.

Both C. garei and C. borealis have, fundamentally, a circumpolar or
alpine-boreal distribution not unlike that of C. vagabunda (p. 87), but
C. borealis has apparently become confined to inaccessible islands and
the European Alps, whereas C. garei is established over quite a wide area.
It seems possible that these species come into direct competition with
each other when they meet in one area and that C. garei is eventually
successful and replaces C. borealis. At the same time one wonders if in
turn C. garei is slowly being ousted by C. gallinae for in the past it may well
have occupied all birds' nests, wet and dry. One can foresee the day
when it will be forced to occupy a more and more restricted habitat
until it has become a very rare flea, entirely confined to ducks breeding
in marshy ground.

THE HEN FLEA, C. galHnae and the grow flea, C. rossittensis (Plates
XIV, XVI, and Map 3). In Britain C. gallinae is the commonest
and the best known of all the bird fleas. It has been recorded from
65 avian hosts in this country and has been found as a straggler on
a number of mammals, such as rats, bats, moles, mice, squirrels and
stoats. Ducks and geese, however, seem immune to its attacks. It is the
flea par excellence of dry aerial nests and occasionally is seen in numbers
which rival the house-martin fleas. Apart from starlings and sparrows
it greatly favours the nests of owls and the crow family. At least once it
has been counted in thousands in a single nest. The general behef is
that C. gallinae was originally a tit flea and certainly it is exceedingly
common in nests of blue tits and great tits. In the domestic fowl it has
found a new host which suits it admirably, for hen coops are relatively
dry and the hens live in close proximity to one another. Sometimes their
sleeping quarters are teeming with this flea and continual scratching
by the birds has a deleterious eflfect on their health and reduces tgg
laying.

In relatively recent years C. gallinae has been introduced into the
eastern United States (see p. 93) where it infests poultry as well as
wild birds. In the western United States the domestic fowl is para-
sitised by an indigenous flea from wild birds — C. niger. It will be
extremely interesting to see if this hardy Christopher Columbus from
Europe wiU continue its spread westwards and finish up by ousting the

112 FLEAS, FLUKES AND CUCKOOS

native flea from the hen roosts of North America — thus emulating the
unattractive behaviour of the human settlers from Europe.

The biology of C gallinae has been studied in greater detail than that
of most other bird fleas. The life span of this species from ^gg to the
adult's death is on an average 450 to 500 days. As we have pointed out
on p. 69 this varies enormously according to the temperature and other
climatic conditions. The weather can affect the life-cycle in many ways.
For example, egg laying falls off in a very dry spell and so does the
proportion of fertile eggs laid.

A nesting box used by blue tits was kept under observation after the
young had flown in June. Three months later the first specimens
of C. gallinae began to emerge and they continued to do so at intervals
until the following April. Thus, as the winter advanced, the fleas
remained for progressively longer periods in the larval stages. This type
of phenomenon has led some people to suggest that fleas can lay fertile
eggs in the absence of a mammalian or bird host and breed for several
generations in this manner. There is no evidence however, to support
this theory, which is pure surmise. On the contrary all the experiments
so far carried out go to prove the reverse. Not only does C. gallinae require
a blood meal before laying, but tgg production is confined to the spring
and early summer.

C. gallinae is one of the species which has been observed leaving nests
in large swarms and as already stated, it is a great wanderer and found
in a variety of strange places far removed from a host or nest. We once
collected a specimen from a plate of soup in Plymouth. This was a
great surprise as most fleas found in such surroundings are cat fleas,
dog fleas and human fleas.

Personally we have no great love for this species which has the
annoying habit of turning up in rare birds' nests, such as those of the
crested tit, or black redstart — even high up in the Alps — and thus
providing a series of disappointments for the collector who is hoping
for something new and strange.

The crow flea is so like the hen flea that anyone can be excused for
mistaking one for the other. Unlike C. gallinae, however, C. rossittensis
is strictly host-specific and is confined to the crow [Corvus corone). It has
been recorded only once in Britain, from a nest in Cumberland,
although its presence here was long suspected owing to its distribution
in Germany and Holland. C. gallinae is the commonest flea in crows'
nests and as the two species are generally present in the same nest, and

FLEAS 113

C. rossittensis in much smaller numbers, the latter can easily be over-
looked.

The host has split into two well marked geographical races. It is
claimed that C. rossittensis can also be divided into two subspecies — one
off the carrion-crow and one off the hooded crow, but the evidence is
meagre and the suggestion must be regarded as tentative. Unfortunate-
ly, no fleas have been found in the nest of the hooded crow in Great
Britain.

The eighth sternites of the males and the shape of the receptaculum
seminis of" the females show features by which C. rossittensis and C.
gallinae can be separated.

THE MOORHEN FLEA, Dasypsyllus gdUnulae, (Plate XIII, and Map 4).
This strange flea which originally hailed from the South American
continent has an isolated position among British bird fleas. It is the
commonest species we have apart from C gallinae and one of the largest.
It is also particularly easy to identify, both sexes being quite unlike any
other of our bird fleas. The two heavy spines, like the horns of an
antelope, on one of the genital flaps of the male can be spotted with a
hand lens, and the deep "bite" out of the seventh sternite of the female
is equally unmistakable.

D. gallinulae is very frequently found in nests with other bird fleas
such as C. gallinae and C. garei, and a closer study of its ecolog)^ would
no doubt prove extremely interesting. It is found relatively more often
on the body of the host compared with hen flea and duck flea, which
are essentially nest dwellers. In Great Britain it has been found
parasitising 59 different species of bird hosts. These are varied, ranging
from the moorhen, woodcock and grouse, to the robin, goldcrest,
willow-tit, and tree-creeper, although generally speaking (seep. loi)
it prefers nests in low positions.

D, gallinulae varies considerably in size and a series of both small
and large specimens will hatch out of the same nest.

THE SAND-MARTIN FLEA, C. styx (Platcs XIV, XVI). This flea
has the distinction of having been mentioned by Linnaeus, but though
recording it in numbers in the nests of sand-martins he mistook it for
the human flea.

114 FLEAS, FLUKES AND CUCKOOS

C. Styx is a large species about 4 mm. in length and is the hairiest of
the British bird fleas. It appears to be a very faithful companion of the
sand-martin, and we know of no colony where its absence has been
established with certainty. It is one of the most suitable fleas upon
which to make studies of population density, sex ratio, hibernation,
migration, breeding cycle, but so far the opportunity has been neglected.
On the continent this species provides one of the extremely rare cases
among fleas of polymorphism. That is to say there are two distinct
morphological forms of the female, each of which shows a characteristic
seventh sternite. This confused Rothschild who thought the second
type of female was a distinct species and gave it another name. The
error was subsequently spotted and the true nature of the "new"
species revealed. Perhaps this second type of female will be turned up
in Britain if it is searched for. Sometimes, however, as in the case of the
well-known polymorphic female butterfly, var. valesina of the silver-
washed fritillary {Argynnis paphia), one form is restricted to certain
localities.

C. Styx swarms in the burrows of the sand-martin and no other flea
seems able to compete with it. Only once has another species been
found sharing a nest in Britain, and that needless to say, was the ubiqui-
tous C. gallinae. On the other hand C. styx seems fairly closely adapted
to life in sand quarries and is not found as a straggler except on the
dipper {Cinclus cinclus). It has been taken four times from this bird, in
considerable numbers, and from widely separated areas. On the whole,
however, it can be considered one of our strictly host specific bird fleas.

It has already been noted (p. 80) that C. styx over-winters in
the nest. It can hibernate either as a pupa or adult. Large numbers
have been observed in burrows immediately before the return of the
hosts.

It has been claimed that certain mammal fleas develop finer and
longer bristles on their legs if they parasitise rodents living in holes in
sandy soil. C. styx certainly has finer and more numerous bristles than
other British bird fleas, and this may be a direct result of the type of
soil in which the birds make their nests. The same can be said of the
closely related species off' the sand-martin in North America. A closer
study of fleas will certainly reveal the effect of other external influences,
besides the rather obvious ones of the temperature and humidity in the
nest.

rr^

-13

C
(J

FLEAS 115

THE HOUSE-SPARROW FLEA, C, fringUlae (Plate XIV, XV). This
species is small and pale and gives an impression of delicacy. It is a
parasite of the house sparrow, not of finches as its name suggests.
Sometimes it is found as a straggler in the nests of other small birds and
it has been recorded from the skylark, great tit and pied wagtail. On
the other hand its presence in the empty nests of starlings, house-
martins, swallows and swifts is no doubt due to the true host's habit of
usurping other birds' nests. When the house-sparrow was introduced
into the United States C, fringUlae was either left behind or failed to
establish itself in the new surroundings, for up till now it has not been
recorded in North America.

The eighth sternite of the male and receptaculum seminis of the
female are quite distinct, but this species is frequently mistaken for the
hen flea (C. gallinae) and published records have, therefore, to be
treated with caution.

THE VAGABOND FLEA, C vdgabunda (Plate XIV, XV). This is
a relatively rare flea found in Britain in the nests of the jackdaw and
rock-dwelling sea birds such as the herring-gull, kittiwake and the shag.
It is apt to wander on to other cliff-dwelling birds and has been recorded
from the peregrine falcon and the rare honey-buzzard in Cornwall and
the raven in Ireland. Inland it has been found only three times apart
from the five records off the jackdaw which are discussed in the section
on distribution. Nests of this bird are easy to collect and it would be of
great interest to see how widely spread C. vagabunda is on the mainland
of Britain. It is well established on jackdaws around Oundle and in
such widely distant localities as Herefordshire, Cornwall and Mid-
lothian.

As we have already noted on p. 87 this flea has broken up into
subspecies, and the British representative, Ceratophyllus vagabunda
insularis, is peculiar to these Islands.

THE SHEARWATER FLEA, Omithopsylla laetUiae (Plate XI, XIII,
XVI, XXXIII and Map 4) . This is the only Pulicid bird flea inBritain
and shares with Orneacus rothschildi the distinction of being peculiar to our
fauna. A glance at Plate XVII will show what a contrast this species
presents with any of our other bird fleas. It is relatively compact, short

FFC— I

Il6 FLEAS, FLUKES AND CUCKOOS

and dumpy, whereas the Ceratophyllid fleas are long and loosely built.
The resemblance between this species and the common rabbit flea
(Plate XI) is also quite obvious, as well as the similarity between the
receptaculum of laetitiae and Hoplopsyllus glacialis, the species ofl* the
arctic hare (Plate XIII). In the section on evolution we have dis-
cussed the origins of the shearwater flea and seen how in the family
Pulicidae the change on to a bird host has accelerated the loss of combs,
and a shift of the bristles on the tarsi.

The common rabbit flea congregates on the ears of the host and has
become a partially sedentary species. It is attached to the skin of its
host by the heavily serrated maxillary lacinia. The shearwater flea has
no such modification of the mouth-parts and, as one would expect, is
free in the nest and on the host's body.

Ornithopsylla laetitiae has so far only been recorded in the burrows of
the manx shearwater and the puffin, in the Scilly Isles, Skomer and
Skokholm Isles, off* the coast of Wales, and Ireland's Eye and the
Great Skellig off' the coast of Ireland. The hosts occasionally nest on
the mainland but so far the flea has not been found anywhere except in
tliese remote islands. The puffin is a popular bird with fleas, six species
having been recorded from it, namely: C. gallinae, C.garei, C. vagabunda,
C. borealisj 0, laetitiae and the common rabbit flea Spilopsyllus cuniculi.
The shearwater on the other hand has one flea only, 0. laetitiae, and it
is probably its true host.

Conclusion

Bird fleas are a small group and their chief interest lies in the fact
that they have transferred from mammalian to avian hosts in compara-
tively recent times. Thus, the evolutionary trends associated with the
change to life in feathers are relatively easy to observe and a gigantic
and instructive field experiment is presented to the naturalist should he
care to avail himself of the opportunity of studying it. The cardinal
need, in the first place, is further collecting. And again further collect-
ing. The first line on which to concentrate is the fleas from ground-
nesting birds, particularly from those species which nest in isolated
island habitats, in holes and caves. The student of bird fleas who
reads Murphy's Oceanic Birds of South America almost expires with

FLEAS 117

frustration as he notes one unique opportunity after the other thrown
away. Scores of nests of rare oceanic birds were dug up out of holes
and examined — but no fleas were collected. It is painful to contem-
plate what a revealing and interesting appendix could have been
written to Murphy's first-rate monograph.

Gnathoncus punctulatus (x 37), a beetle
which lives in birds' nests and feeds on fleas

CHAPTER 8

FEATHER LICE (MALLOPHAGA)

(/xaAAoV^WOOL, </)ayos'= eating)

Tell me what company thou keepest, and I'll tell
thee what thou art

Cervantes

THERE WERE no Hcc in the Garden of Eden. Such loathsome creatures
must have been created after the Fall. " Can we believe that man
in his pristine state of glory, and beauty, and dignity, could be the re-
ceptacle and prey of these unclean and disgusting creatures?" So mused
Henry Denny when compiling his Monographia Anoplurorum Britanniae,
the first and only book to be written on the Mallophaga of Britain. To-
day, it is generally believed by entomologists that the feather lice are
derived from free-living ancestors which were not unlike the Psocida or
book-lice in form and habit. These ancestral Mallophaga probably lived
under moss and stones and on the bark of trees, feeding on any organic
debris they could find. Book-lice have been taken from the bodies of
caged animals, such as white mice, where they were possibly feeding on
skin debris, and it is not difficult to imagine that the free-living ancestral
Mallophaga might have visited the bodies of resting reptiles. When the
reptiles which gave rise to the early birds gradually evolved a feather
covering, a hitherto untouched source of food became available.
Originally, feathers must have proved a hard and indigestible diet, but
one which enabled the insect to occupy a new habitat with an almost
unlimited food supply and without competition. Gradually the
ancestral Mallophaga became more and more closely adapted to these
new conditions so that eventually they could live and breed only in the
warmth and shelter provided by the body of their host. The Mallo-
phaga, the feather or chewing lice, are found on all birds and many
mammals, but not on man. It is usually believed that they first became

ii8

FEATHER LICE I I9

parasitic on birds and later spread to mammals, but here we are con-
cerned only with the species living on birds.

Habits And Structure

To the naked eye the Mallophaga are not unlike small free-living
insects. Actually, however, considerable structural modifications have
taken place : chief amongst these is the general flattening of the body
(dorso-ventrally, not from side to side as in the flea), which enables the
insect to sHp between the feathers and to apply itself to their flattened
surfaces for the purposes of feeding and attachment. The head,
especially, has become modified. In a free-living insect, such as the
cockroach, or in an animal Hke a horse, the longer axis of the head hes
at right-angles to the rest of the body. In the Mallophaga the head has
become flattened from top to bottom so that the longer axis Hes in the
same plane as that of the body. The head is a hollow box-like structure
with thickened walls; these have thinner areas (or sutures, Plate XXI)
allowing a Hmited mobihty of the parts of the head for feeding. On the
inner surface of the walls are various thickened ridges (Plate XXI)
which give strength to the head and form a supporting framework for
the mouth-parts. These sutures and ridges are useful characters in
classifying the genera of the Mallophaga.

The feather hce, unhke the fleas, show considerable diversity in size
and general body form (Plates XXII-XXIII) . This diversity has been
brought about by the Mallophaga occupying the different types of
habitat, such as the head and the wings, found on the body of the bird
and becoming speciahsed and adapted for life in these locations.

In size feather Hce range from the minute game-bird-infesting
Goniocotes, in which the males are just under a millimetre in length —
a Htde less than the proverbial pin's head— to the large hawk-infesting
Laemobothrion which may be up to ten millimetres (about one-third of
an inch) in length.

Feeding, The Mallophaga, originally feeders on various kinds of
organic debris, took to eating feathers when they became parasitic on
birds. This change of diet did not necessitate any fundamental modi-
fications in the original chewing mouth-parts, which were probably
similar to those found in an unspecialised insect Uke the cockroach.

120 FLEAS, FLUKES AND CUCKOOS

The strongly-toothed, dark-coloured mandibles (Plate XXI) can be
seen either near the centre of the head (Ischnocera*, Plate XXII) or
near the anterior margin (Amblycera* Plate XXII). These are used
to cut off pieces of feather, usually of constant lengths, which fall into
the pouch-like labrum or forelip. Movements of this pouch force the
food into the mouth. The maxillae and labium are reduced to simple
lobes either without palps (Ischnocera) or with segmented maxillary
palps (Amblycera), and probably play only a minor part in the feeding
operation.

The feather-feeding forms generally take the down or downy
part of the larger feathers. When feeding the louse approaches the barb
of the feather head foremost and hangs to it by the second and third pair
of legs, the first pair being used to direct a single feather barbule
towards the mandibles. The pieces of feather, cut by the mandibles
and forced into the mouth by the labrum, pass down the oesophagus to
the crop. When full this shows as a black structure lying in the abdo-
men of the living insect, rounded anteriorly and pointed posteriorly
(Plate la). If a louse is watched while feeding, strong pulsating move-
ments of the crop can be seen. These movements help in the breaking
up of the feather parts, particularly by rubbing them against sets of
comb-like structures in the wall of the fore-part of the crop. Small
mineral granules are sometimes found in the crop, and it has been
suggested that these may act as further grinding agents — an interesting
analogy to the grit in the gizzard of the bird. But more than purely
mechanical treatment is needed for the digestion of the food. Feathers
consist mainly of keratin — a strongly resistant substance — and before
this can be acted on by the digestive enzymes of the gut it must be
subjected to a strong reducing agent. Such an agent is secreted in the
stomach of the louse; the larva of the clothes moth, which also feeds
mainly on keratin, secretes a similar substance. The protein-digesting
enzyme of the louse is also adapted to enable it to digest the specialised
protein of the keratin, when the latter has been broken down by the
first secretion.

Some of the feather-lice harbour bacteria, which are confined to
special cells lying in groups in various parts of the body. Elaborate
methods have been evolved by which the bacteria infect the breeding
organs of the female and are passed into the egg^ thus ensuring the
continued association between bacteria and louse. The exact role
♦See p. 139 for explanation of these superfamilies.

FEATHER LICE 121

played by these bacteria is unknown, but it has been suggested that they
are in some way associated with the digestion of the specialised diet of
the feather Uce. Among the bird Mallophaga, these are found chiefly
in the superfamily Ischnocera, which are mainly feather-eaters, and
only rarely in the superfamily Amblycera which take blood and other
substances in addition to feathers. This fact actually makes the problem
more confusing as similar bacteria are found in the sucking lice (Ano-
plura), the bed-bugs {Cimex), the fleas (Aphaniptera), the ticks and
certain mites (Acarina) which are all true blood-suckers. It has been
shown, for instance, that nymphs of the sucking louse of man (Pediculus
humanus) cannot survive if deprived of their bacteria.

Some Mallophaga (of the superfamily Amblycera) may live entirely
on blood and serum, or add this to a mainly feather diet. One of the
chicken lice (Menacanthus stramineus) , which hves on a mixed feather and
blood diet, uses its mandibles to puncture the young feathers in quill and
to take the blood from the central pulp supplying the growing feather.
Its oesophagus is provided with strong muscles and can exert a sucking
action. This species also gets blood by gnawing through the skin of its host.

The members of one genus of Mallophaga {Piagetiella) Hve attached
to the inner walls of the throat pouches of pelicans and cormorants,
where their diet must consist of blood and serum, and possibly epidermal
debris taken from the walls of the pouch. Another species {Actornitho-
philus patellatus) spends part of its life-cycle inside the shaft of the flight
feathers of the curlew (Plate lb), probably feeding on the dried feather
core. The nymphal stages of one of the species [Dennyus truncatus) found
on the swift are said to live on the liquid secretions of the eye of the
host. It is doubtful whether any species subsist entirely on epidermal
scales and other debris found on the surface of the body of their host,
but it is probable that some species, in addition to their normal diet, do
undertake a certain amount of general scavenging. In the crop of one
louse which he examined Waterston found granules of mica and quartz
a butterfly scale, part of a seed coat, a minute fungus, its spore and a
fragment of feather. Crops have also been found containing empty
Mallophagan ^gg shells, cast larval skins and parts of mites and other
lice — this suggests that the Mallophaga may, at times, indulge in
cannibalism.

Locomotion and Sense Organs, Feather lice, as would be expected from
the diversity of their body form, show considerable variation in the

122 FLEAS, FLUKES AND CUCKOOS

speed and manner of their movements. Most species can run backwards
and forwards with equal facility; the short round forms (Plate XXI)
living on the head and neck do not move great distances, but can slip
speedily out of sight into the down at the base of the feather; the narrow
elongate forms found on the larger feathers of the body and wings, are
fast movers and able to slip sideways across the breadth of the feather
and from feather to feather with great rapidity.

The legs are comparatively uniform throughout the bird lice. In
the Ischnocera they are adapted for clinging to the feathers by means of
the shortened tarsus and paired tarsal claws (Plate XXI). In the
Amblycera, which move more generally over the surface of the body
and feathers of their host, the legs have a longer tarsus, and are able,
through a modified part of this segment, to cling to smooth surfaces ;
thus they can climb up the sides of a glass tube, whereas the Ischnocera
cannot do so.

The Mallophaga are photonegative and have a positive reaction to
the warmth and the smell of their hosts, reactions which ensure that the
lice keep well within the plumage, and do not stray off their hosts on to
other objects which may come within reach. On the death and corrup-
tion of the host, when the stimuli of temperature and smell undergo a
change, the lice come to the surface and can be seen moving restlessly
over the feathers.

Their eyes are probably only able to perceive the difference between
light and darkness, and the movement of other objects. Each eye is
protected by a sensory hair (Plate XXI) which serves as a tactile
sense organ, probably helping to guide the louse in its passage through
the feathers.

The antennae (Plate XXI), which can be seen in a constant state
of motion in the living louse, are also used as tactile organs in the
Ischnocera and in some of the Amblycera, but in this latter group they
may be small and completely enclosed in a fold of the head. They also
bear sense organs which are possibly connected with the perception of
warmth and smell similar to those in the antennae of the sucking louse
of man. The male antennae (in the Ischnocera) may be used to clasp
the females during copulation, and in some species (Plate XXIIIa) they
are larger than those of the female and have hook-like appendages
which improve their efficiency as clasping organs.

All parts of the body bear numerous hairs or setae which are supplied
with nerve fibres, and serve as further tactile organs.

FEATHER LICE I23

Life History. The complete life history, from tgg to adult, takes place
— unlike that of the flea — on the body of the host. Not much is known
about this aspect of the biology of the Mallophaga. The female is almost
always larger than the male, and in many species the numbers of this
sex in any one population are greater than those of the males, and in
some, which have been widely collected, males have rarely or never
been found. The development of the egg without fertilisation (i.e.
parthenogenesis) is known to take place in one of the mammal lice, but
the extreme rarity of the males in some species and the normal apparent
excess of females over males, could also be caused by the immediate
death of the male after mating.

The life history has been studied extensively only in the common
pigeon louse {Columbicola columbae)^ and most of the following account
refers to this species.

The eggs when first laid are pearly white, and are fixed to the
feathers with a cement-like substance secreted by a special gland
associated with the female reproductive organs. In Columbicola and
other species living on the wings they are laid in rows, end to end, along
the grooves between the barbs of the flight feathers and under wing
coverts (Plate XXIV) ; in this position they are protected by the edges
of the grooves and so escape damage by the bill of the bird during wing
preening. The other main egg-laying site is on the feathers of the head
and neck, where again the eggs are safe from the preening bill; here
they are laid singly or in clusters near the base of the feather. In heavily
infested birds the eggs may be found attached to feathers almost any-
where on the body, and some of the Amblycera normally lay their eggs
on the feathers of the breast and belly. The curlew quill louse, like the
quill mite, lays its eggs in a spiral column on the inner wall of the quill.

Each egg has a cap (or operculum), separated from the rest of the
tgg by a line of weakness ; any pressure applied to the egg will cause a
break at this point. The eggs may be objects of some beauty, adorned
with various reticulate surface sculpturing and plume-like processes on
and around the cap. The normal rate of egg-laying is unknown; a
female Columbicola kept in captivity at optimum temperature and
provided with pigeon feathers, did not average more than one egg
every two or three days. The time taken for incubation probably varies
in different species. In an incubator at a temperature of 37°G. the
eggs of Columbicola hatch from three to five days after laying; lowering
of the temperature may prolong the period to fourteen days. Nymphs

124 FLEAS, FLUKES AND CUCKOOS

kept at 33°G. only live a few days. Temperature of the host, therefore
affects not only the length of the life-cycle, but also the survival of the
young, and may be one of the limiting factors in the establishment of a
louse on a new host (see discussion under host specificity, p. 137).

When the nymph, within the egg^ is ready to hatch it begins to suck
in air through its mouth; this air passes through the alimentary canal
and accumulates in the egg-shell behind the nymph. After about five
minutes of this sucking action the pressure of the air behind the nymph
becomes so intense that the cap or operculum of the egg is forced open.
During the next twenty minutes the nymph frees itself from the egg
shell by muscular contractions, expansion of the abdomen and further
pumping of air. It can at once move freely about on the feathers, but
food (which is the same as that of the adult) is not taken until several
hours after hatching.

The feather lice, unlike the fleas, have no metamorphosis. The
nymph which emerges from the egg resembles the adult in habits and
general body form, differing in its smaller size, absence of colour, un-
developed sex organs, and certain other morphological details. The
nymph sheds its entire skin three times before reaching the adult state.
In Columbicola each stage lasts from six to seven days, and after each
moult the nymph becomes successively larger, darker and more like
the adult. Nothing is known about the length of life of the female or the
total number of eggs she lays. But far fewer eggs are required by ecto-
parasites which spend generation after generation on one individual
bird, than by those in which the young are faced with the risky business
of finding a new host after hatching.

Host and Parasite

Population Size of Parasite and Effect on Host. The number of lice (or
population size) found on any one bird varies considerably from indi-
vidual to individual, even in the same species. This variation does not
seem to be entirely seasonal; a number of birds of the same species can
be examined at the same time of year, and some may be lightly infested,
some heavily infested and some altogether louseless. Certain species, for
example rooks and crows and some of the waders, have a higher propor-
tion of both infested individuals and individual lice, but even amongst
these, lice-free birds may be found. A curlew from Ireland, in excellent

FEATHER LICE I25

condition and plumage, was found to have 1,803 ^ice, another from
Suffolk, 1,047, and a rook from Wiltshire just over 300. These numbers
are unusually high, although the curlew is always found to harbour
some lice, usually between 50 and 200. In the case of the small passer-
ines, many individuals seem to be louseless, or the numbers found are
small, usually between one and ten in number — over twenty lice is
uncommon. Young birds tend to be more heavily infested than adults
and sick birds more than healthy ones. The world record is held by an
East African cormorant [Phalacrocorax nigrogularis) which harboured
over 7,000. It is doubtful if there is any species of bird in the world
which is without at least one kind of feather louse. This pained the
early entomologists, one of whom remarked that "even the gorgeous
peacock is infested by one of extraordinary dimensions and singular
form"; and Benjamin Franklin ruefully laments the choice of the bald
eagle as the emblem of America : "as he is generally poor and often
very lousy."

The population of lice may be large without apparently harming
the bird, but when it is abnormally heavy, in sick, captive, or young
birds, the effect on the host may be serious. The mere movement of the
lice is intensely irritating, so that the bird damages itself by excessive
scratching. The lice, if too numerous, may denude some of the feather
shafts, and cause injury and loss of blood by rupturing the skin during
feeding. The punctures made in the feathers when in quill, by the
chicken louse, may inhibit their development altogether.

The Mallophaga, up to the present, have never been convicted as
effective carriers of any disease, a fact which is reflected in the small
amount known about their biology compared to the typhus-carrying
sucking louse and the plague-carrying flea. One of the mammal
Mallophaga, that of the dog, acts as the intermediate host of a tape-
worm; and there is a single record of a bird Mallophaga [Dennyus]
acting as the intermediate host of a roundworm {Filaria), which
parasitises the bird host, a swift. Further work may reveal other cases
of parasites which spend part of their life-cycle in the host and part in
the louse.

Factors Limiting Population Size. The fact that birds tend to be
more heavily infested if they are sick suggests that, by their own
efforts, they normally help to keep the louse population in check.
Preening by the bird (Plate VIII) doubtless eliminates a number of

126 FLEAS, FLUKES AND CUCKOOS

Mallophaga and their eggs, and tends to restrict egg-laying mainly to
the head and neck, or to a modified form on the wing feathers. A
specimen of the cuckoo head louse {Cuculoecus latifrons) was recently
found on the back of a cuckoo in a damaged condition — the thorax and
abdomen being attached to one feather, and the severed head to an
adjacent one. The louse presumably had strayed from the safety of its
normal habitat, and was torn in two during the preening of the back
feathers. Further evidence of the importance of preening is shown by
the case of a robin which had most of the upper mandible of the bill
missing; it was infested with 127 specimens of Ricinus rubeculae, the
numbers of which rarely exceed 15 on any one bird.

The choice of habitat, the structural modifications of the louse and
the position of the egg-laying sites, have probably been largely deter-
mined by the preening habits of birds. It is interesting to speculate
whether the apparent colour adaptations of some lice to the feather
background on which they live are true cases of adaptive colouration.
Are they protected from the bird in the same way as the woodcock,
whose plumage merges with the dead leaves and bracken amongst which
it lives, is protected from carnivorous predators ? There are many
instances of a resemblance between the colour of the louse and the
plumage of its host: white lice on the white gulls and darker lice on the
darker but related skuas ; white lice on the white swan, dark lice on the
black swan; a yellow louse on the golden oriole, a black one on the
coot. Such examples could be multiplied almost indefinitely. It has
been suggested that the yellow colour of the golden oriole louse is due
to the fact that it eats the substance which gives the feather its yellow
colour. There is no proof of this, and it is an explanation which cannot
be applied to such cases as the white swans and gulls, which in addition
to lightly coloured lice, also have other species which are brown and
sometimes exceptionally dark in colour. These dark species, it should
be noted, are confined to the head and neck where they are out of reach
of the beak. It seems probable that certain genera of feather lice, like
the last nymphal instars of the human sucking louse, have the ability to
respond to the colour of their background. It is not known, however, if
the resulting similarity in colour between the louse and the feather on
which it lives does in fact serve a protective purpose.

Bathing in water and dust and the subsequent preening (Plate VIII)
helps the bird to rid itself of parasites. Lice have been found in the
dust taken from dust baths habitually used by chickens. As Pliny

FEATHER LICE I27

remarked, " These insects . . . are apt to kill the pheasant unless it takes
care to bathe itself in dust."

The phenomenon known as "anting" may be another method by
which the bird keeps down the numbers of its lice. Russian soldiers were
said to clean their lousy garments by putting them on ants' nests, and it
has been suggested that the habit of some birds of lying with outstretched
wings on an ant's nest allows the ants to run through their plumage and
perform a similar service. The subject, however, is both controversial
and complicated. There are two types of anting behaviour, one known
as "passive anting", the other as "active anting". " Passive anting "
by a young carrion-crow is described by Condry : "After a few seconds
hesitation he stepped into the middle of the swarming ants . . . When
some of the ants found their way via his legs to his feathers, the bird
showed apparent pleasure and slowly settled down among the ants with
wings outspread and tail fanned. Then he dropped his head down in a
swooning posture till his beak touched the ground. He was soon covered
with ants ..."

Many cases of "active anting," which seems to be a more usual
phenomenon, have been recorded : Chisholm describes this curious
procedure carried out by some immature starlings :

" Each bird snatched up an ant from a gravel path and dabbed
it quickly first under one wing and then under the other, after which
the insect usually was dropped . . . All the actions of the starlings
were very rapid. Two birds in particular nearly fell over backwards
while rearing up smartly and applying ants beneath their tails . . .
When the birds departed, the path was bespattered with dead and
maimed ants, some fifty per cent, of which had their abdomens
burst."
There is further evidence which may throw some light on this
peculiar habit. Tame or captive birds have been seen rubbing cigar-
butts, lemon-juice, vinegar and even beer into their plumage. The
American purple grackle {Quiscalus quiscula) anoints its plumage with
the liquid found inside the walnut, which has a strong acid reaction,
and there are other reports of birds applying aromatic oils from fruits
and leaves to their bodies. It has therefore been suggested that the
birds are smearing insecticides on their plumage. The formic acid
within the bodies of the ants is liberated as these are crushed against
the feathers, and it is thought that the lice and other ecto-parasites are
either killed directly, or through eating the acid-covered feathers.

28 FLEAS, FLUKES AND CUCKOOS

Some biologists, however, believe that the birds merely get an enjoyable
sensual pleasure from the movements of the ants among the feathers, or
from the stimulus of formic acid on the skin. It is a well-known fact
that tame parrots and owls enjoy having their necks tickled. One tame
parrot developed the habit of pushing a piece of apple under its wings
or into the back between the shoulders; it was suggested that the acid
in the apple cooled or stimulated the skin. Finally those who favour
the theory of odour-attraction believe that the bird is scenting itself and
that the smell of the formic acid or aromatic oils are a source of pleasure
and satisfaction. Although there is as yet no conclusive explanation
of the habit of "anting," Chisholm, who has studied and reviewed the
subject (1944), considers that the value of the acid as a skin stimulant
is the most potent factor. An indirect result which springs from the
presence of acids on the feathers is the death of the parasites. It
seems possible that the habit may have arisen from birds taking dust
baths in the loose earth found on ants' nests, and the additional
stimulus and cleansing power of the formic acid was appreciated.
Again, many birds when sunning themselves take up the passive anting
position (Plate IVb) and the habit may have been initiated by birds
sunning themselves in the vicinity of ants' nests. " Howe handsome
it is to lye and sleepe, or to lowze themselves in the sunn-shine."

Little definite information is available about any other factors
which limit population size. There may be competition between the
different species on one host (interspecific competition) or between
the individuals of one species (intraspecific competition). Waterston
records finding a specimen of Goniodes (a large louse from game-
birds) with its crop crammed with pieces of Goniocotes, a consider-
ably smaller louse. Mites, when numerous, may also keep down the
number of Mallophaga, possibly by the destruction of the eggs, for
empty egg-shells have been found occupied by mites.

Little is known about the diseases which attack the Mallophaga.
Occasionally parasitic fungi have been observed in the form of colour-
less club-shaped projections on the bodies of the larger lice, and it is
probable that they are in some way harmful to the host. Mites and their
eggs are also found attached to feather lice. These mites, which belong
to a genus peculiar to the Mallophaga and closely related to another
genus found on the louse-flies, have been recorded from Trinoton
(Plate XXII) and Ancistrona only, which are particularly large in size.
They seem to be relatively harmless. Thus in the case of some of the larger

FEATHER LICE 129

feather lice at any rate, Addison's remark is justified : "A very ordin-
ary Microscope shows us, that a louse is itself a very lousy Creature."

Origin — Evolution — Classification

If the photographs of Mallophaga in this book are shown to an
expert he can say after a superficial glance from which order of birds each
specimen was collected. Similarly if you were to show the expert a
louse and say : "I took this off a snipe," he might reply : " Yes, but
that day you also shot a partridge and put it in your game bag with the
snipe." This is possible because groups of related birds — say the game-
birds, the waders, the hawks — each have their distinctive types of lice.

Close correlation between bird and parasite can be explained
by the theory that birds were parasitised at an early stage of their
evolution, before they had diverged greatly from the generalised
ancestral type. As the birds evolved and became adapted to different
environments and ways of life, there were modifications and changes in
their body form, in the physical structure of the feathers, and in the
temperature and secretions of the body. The Mallophaga,
closely associated as they are with the surface of the body and the
feathers, had to become adapted to these changes. Each step, therefore,
that took a group of birds further away from the ancestral type and
from other evolving groups, was followed by the Mallophaga living on
it. The morphological changes in the feather lice, however, were slower
and less drastic than in their hosts, and the differences between any
of the Mallophaga are now less than those between say a penguin and
a peacock. The environment of the Mallophaga is formed mainly by
the external characters of the bird — the feathers and skin texture —
together with the temperature and secretions of the body. The changes
in this environment were probably smaller than those in the external
environment of the bird, and the resulting modifications in the structure
of the louse are, therefore, less. It is also possible that the Mallophaga
after an initial evolutionary spurt became more stable, in the evolution-
ary sense, than their hosts, and thus remained more constant in form.

This slower rate of evolution in the Mallophaga is the reason why
they have changed less than their hosts, and have retained more
characters which show their relationship to each other. The curlew and
the oyster-catcher, both waders (Charadrii), belong to different families

130 FLEAS, FLUKES AND CUCKOOS

(Scolopacidae and Haematopodidae) ; but the head hce of these two
birds are more similar, being closely related species of one genus —
Saemundssonia. Again, the three suborders of the Charadriiformes —
the waders (Charadrii), the gulls (Lari) and the auks (Alcae) contain
birds which differ greatly from each other in appearance and habits,
but their head lice are similar and can be placed together in the genus
Saemundssonia. As we would expect from our theory of evolution, how-
ever, the head lice found on the curlew, for instance, are more like
those of other waders (Charadrii) than those of either the gulls (Lari)
or auks (Alcae).

The evolutionary story of the birds is sometimes pictured in the
form of a tree. The trunk represents the ancestral stock, giving rise to
branches, which themselves branch and branch again ; the subdivisions
of one branch being more closely related to each other than to those of
any other original branch. The larger subsidiary branches may be
taken to represent the orders, such as the game-birds (Galliformes) or the
ducks, geese and swans (Anseriformes), with the smaller branches as
families and genera down to the twigs which represent the species. If
we place a similar evolutionary tree for the Mallophaga against this one
we shall find that a branch representing a genus of Mallophaga will not
correspond with a branch representing a genus of birds, but may, like
some straggling piece of ivy on an elm, cover all the subsidiary branches
forming an order of birds. Thus, in a great many cases there is a genus
of Mallophaga which is found on one order of birds and no other. For
example, the Ciconiiformes (the storks and herons) harbour five genera
of lice found on no other birds ; the Procellariiformes (petrels) have ten
and the Galliformes (game-birds) have at least seven genera of lice
which are peculiar to them. Hence it follows that by examining a
bird's Mallophaga it is often possible to say to which order the bird
belongs.

In addition to these genera restricted to one order of birds there are a
number parasitising birds belonging to two or more, often quite
distantly related orders. The presence of such genera cannot be ex-
plained solely by this particular evolutionary theory and certain other
factors must be considered before we can even try to understand the
complications of the present day distribution and relationships of the
Mallophaga.

INTERNAL THICKENED RIDGES

LABRUM.

HEAD ^

ANTENNA--

EYE '

^. OCULAR SETA-''

THORAX <

ABDOMEN •{

Plate XXI

SUTURE

-MANDIBLES
LABIUM 8c

"maxillae

CLAWS

SETAE

J. G. Bradbury

Head feather louse, Saemundssonia sp., from common tern, showing important

characters ( x 46)

\V. H. Pollen

a. Amblycera: Trinoton sp., from duck
( ^ 19^

\V. H. Pollen

b. Ischnocera: Pectinopygus sp. from
cormorant ( x 34)

Plate XXII THE TWO MAIN TYPES OF FEATHER LICE

FEATHER LICE I3I

Ecological Niches. If the louse population of any individual bird is
examined it is evident that this comprises a number of quite different
types of Hoe. Each of these is distinguished by habits and general body
form and most birds are found to harbour five or six, some even up to
twelve of these different genera. This diversity of lice can be explained
by the theory of ecological niches.

It is a truism that no place which can support life is without Hfe.
Every possible habitat and source of food — that is, every ecological
niche — will be utilised by some form of organism. It can be stated
broadly that all the higher categories of classification, such as the orders,
are based on the original divergence of the ancestral stock to fill
available ecological niches. The order Anseriformes (ducks, geese and
swans) is descended from a line which became adapted to life in the
water, and the Ciconiiformes (storks and herons) from one that became
adapted to life in swamps and marshes.

We have seen that the reptile-like ancestors of the birds developed
feathers and thus produced a new type of environment— an empty
ecological niche. This was occupied by a primitive free-living insect
which gave rise to the parasitic bird-lice of to-day.

The invasion of any new territory, where food is unlimited and
competition absent, seems to act as a great stimulus to evolution. ^ The
primitive, unspecialised, ancestral Mallophaga finding such a territory,
must have rapidly filled the ecological niches then available on the
body of the host, and also those formed subsequently through the
differentiation of the plumage during the evolution of the birds. The
occupants of each ecological niche diverged from one another as they
became specialised and adapted to the particular environment in
question — whether of the head and neck or wings and back. In the
same way the marsh dwelling birds with their long legs, long necks and
long pointed bills which adapt them for life in that particular ecological
niche, differ from the birds of the ponds and lakes, with their short legs,
webbed feet and flattened beaks.

Looking at the louse population of most birds it is a simple matter
to pick out the lice adapted to two of the ecological niches, namely,
those of the head and of the wings and back. The Mallophaga living
on the head and neck, where they are out of reach of the bird's beak,
have less need for rapid movement and have become adapted to a
comparatively sedentary life on the feathers. The abdomen is short
and round and not particularly flattened, the legs are short with strong

FFC— K

132 FLEAS, FLUKES AND CUCKOOS

claws adapted for clinging to the feathers, and the head large to accom-
modate the heavy strong mandibles and their supporting framework
(Plate XXI). Such fat-bodied forms on other parts of the body
would be easily picked off by the bird or crushed by its bill. The eggs
are laid on the feathers of the head and neck, singly or in bunches, and
need no special modifications to protect them as they are out of reach
when the bird is preening.

On the wings and back, where the louse is always in danger from
the bill, a flattened elongate, long-legged type is found (Plate XXI lie)
which is able to move rapidly, mainly by slipping sideways across the
feathers. The eggs, which are laid on the wing feathers, are elongated
and usually placed between the barbs, which protect them during
preening.

Apart from these two extremes — the large-headed, short-bodied and
the flattened elongate forms — there are many others which are
intermediate in body form and have different habits. These presumably
occupy different habitats on the bird, but our knowledge of the ter-
ritory- of the majority of lice in general is lamentably small. In
some birds, such as the common mallard, there is one head louse
{Anatoecus) and one wing louse (Anaticola) , but in other birds there may
be two or more genera occupying the same habitat. In the game-birds,
for instance, there are two genera apparently adapted to life on the
wings.

The Mallophaga we have just been discussing belong to the super-
family Ischnocera (Plate XXII). The majority of birds also harbour one
or more species of genera belonging to the other superfamily, the Am-
blycera. The members of this superfamily have, in general, become less
closely adapted to particular habitats on the bird's body. They are nearly
all fast runners and probably move freely all over the host's body, and are
not specialised for life on particular feathers. This absence of specialisa-
tion results in less well marked divergence, and the Amblycera are thus
divided into far fewer genera than the Ischnocera. Using the term
genus in its broad sense the Ischnocera are represented by about forty
genera on British birds and the Amblycera by twenty-two. Again, if the
nine genera found on the British game-birds are considered, we find
that six of these belong to the Ischnocera and only three to the Ambly-
cera. It is usually believed that the Amblycera have retained more of
the habits and hence the morphological characters of the primidve
ancestral Mallophaga. The most specialised character of the Amblycera

FEATHER LICE 133

is the fold of the head, which envelops the antennae, and is probably
a modification to protect these structures when the louse is moving
rapidly through the feathers. A somewhat similar device is found in
several other groups of ecto-parasites.

Two unusual ecological niches have already been mentioned — the
throat-pouches of pelicans and cormorants occupied by the genus
Piagetiella and the quills of the wing-feathers of the curlew by a species of
Actornithophilus . The fact that these two are members of the less specialised
Amblycera suggests that the occupation of the two niches is compara-
tively recent. The limited distribution of the pouch-louse within the
order Pelecaniformes and of the quill-louse within the order Charadrii-
formes also supports the idea of a relatively recent colonisation of these
two habitats.

Many of the problems confronting systematists are caused by
animals leaving their original ecological niche in favour of another.
They subsequently develop characters which adapt them to their new
environment : these are superimposed upon, and more or less obliterate
the original characters which would form the basis for their scientific
classification. The flamingoes probably illustrate a case of this kind.
They are placed by most ornithologists with the storks and herons, but
by a few with the geese and ducks. There are convincing arguments to
support each theory. The evidence provided by the Mallophaga on
the systematic position of these long-legged ducks or duck-billed storks
will be discussed later. Our knowledge is still insufficient to enable us
to recognise all the genera of Mallophaga which have possibly changed
their ecological niches, but there seems little doubt that this has
happened in the case of one genus on the passerine birds. The head
louse {Philopterus) of passerine birds is a typical inhabitant of the head
niche — with a short round body and large head (as in Plate XXI).
The starlings, however, lack a typical passerine head louse, but a
species (Plate la) is found on the head which resembles it in general
body form. A detailed examination of this species shows that it is, in
fact, more closely related to another genus of body louse with a small
head and a more elongated body, also found on the passerines. It is
tempting to speculate that the original passerine head louse on starlings
became extinct, for some unknown reason, and that the empty ecologi-
cal niche was filled by members of another genus which have now
assumed the general body form of a typical head louse.

134 FLEAS, FLUKES AND CUCKOOS

Convergent and Parallel Evolution. The case just described is an example
of convergent evolution. That is to say, a louse which is not closely
related by recent common ancestry to other head lice has assumed
similar characters in response to the same environment. Their resem-
blance thus indicates a similar history rather than a similar ancestry.
Problems caused by convergent evolution may be responsible for many
of the difiiculties in the classification of the Mallophaga. Sometimes it
is relatively easy to unravel these relationships, but if sufficient time has
elapsed to enable the new occupant to adapt itself along closely similar
lines so that it comes to resemble the original inhabitant of the niche,
mistakes can easily be made. It is consequently difficult to decide
which characters in the louse indicate relationship or derivation from a
common ancestor, and which are developed as a result of living in the
same environment. On many birds the lice belonging to different
genera will show a number of similar characters. Some of these, without
doubt, are developed as a response to the type of feathers forming the
plumage of the host. The lice living on birds with iridescent feathers,
for instance, sometimes have a thicker exoskeleton with a sculptured or
pitted surface.

Another factor which may be responsible for some of the present
confusion in the classification of the Mallophaga is so-called parallel
evolution. This term is used to describe a case where two primitive
stocks office, after diverging, have evolved along similar lines. Parallel
evolution is, therefore, the independent acquisition by related groups of
similar characters during their evolution. In contradistinction, con-
vergent evolution is the acquisition of similar characters by unrelated
groups in response to a similar habitat — the whales and the fish being a
well known example. It is often difficult for the parasitologist to decide
whether two groups of species are strikingly alike because they are close
relatives or whether the likeness is due to parallel evolution.

Discontinuous Distribution. Discontinuous distribution is a term used
to describe populations of animal species which are divided from one
another by large geographical areas in which their own kind is totally
absent. It is believed that many animals which once had a continuous
range over a wide geographical area, such as Europe, have become
extinct in parts of this range, leaving isolated populations here and
there. Since isolation is an important factor in species formation (see
p. 1 38) these animals may evolve into new species or even new genera.

FEATHER LICE 1 35

On the other hand if the extinction of the intervening populations is a
recent phenomenon and, if at the time of their isolation, the species was
for some reason stable in the evolutionary sense, there will be a clear
case of discontinuous distribution. Although the term is generally used
in connection with free-living animals it can equally well be applied to
the host distribution of permanent parasites. It can also be applied to
the distribution of genera as well as species, for some genera are confined
to specific geographical areas, whereas others show a world-wide distri-
bution. The distribution of certain genera of Mallophaga can only be
explained by assuming that these are stable genera which were once
found on all birds, but have now become extinct on some orders. The
genus Laemobothrion is found on the storks, the rails and the hawks;
Colpocephalum is found on eleven out of the twenty-seven orders of birds,
ranging from pelicans to passerines. Thus, the species of these genera
must have remained relatively stable throughout a vast expanse of
geological time. It is generally accepted that most of the present
families of birds were in existence by the Upper Eocene, some forty-five
to seventy million years ago, and such a widely distributed genus as
Colpocephalum must have already been living on the ancestors of these
families.

The Species and Host Specificity. If we return to our expert with another
louse he can tell us not only that it is a parasite of a game-bird, but also
that it came from a partridge and not a pheasant. In other words
many birds have host-specific lice (see p. 43) . Occasionally it is easier
to distinguish two lice from each other, than to separate their respective
hosts : the common and arctic terns, which are often confused, harbour
species of lice which, in the males at least, can be separated with ease.
In other cases one species of louse may be found on two or more related
birds.

Host specificity in the Mallophaga, at least in some cases, is now
firmly established. The lice of parasitic birds such as the cuckoo clearly
demonstrate this fact. The cuckoo is reared by foster parents and their
lice have ample opportunity for passing to the young bird. This does,
in fact, occasionally happen : two specimens of a louse normally in-
festing a passerine bird were found on a young cuckoo, probably still
being fed by the fosterers. If there were no host specificity the lice of the
foster parents could have established themselves on the cuckoo and
might even have replaced the original cuckoo lice. If this happened the

136 FLEAS, FLUKES AND CUCKOOS

cuckoos of the British Isles would have no particular species of lice, but
they would be parasitised by a variety of passerine-infesting species.
This however is not the case. The adult cuckoo in England is infested
by three species of lice belonging to the genera Cuculoecus, Cuculicola and
Cuculiphilus , which, as their names imply, are true cuckoo-infesting
genera found on species of the cuckoo family throughout the world,
but not on the Passeres. Thus, although the lice of the passerine
foster parents have ideal conditions for transference — continuous
contact and no competition — the host specificity already developed
makes establishment on the new host impossible. There is no satis-
factory explanation of how the cuckoo acquires its normal lice. In
most birds the lice can pass from the parent to the young in the nest,
but in the case of the cuckoo contact between individuals takes place
only during mating, and it must be presumed that the lice are usually
transferred at this time. Transport by louse-flies (further discussed
below) in the cuckoo's winter quarters may be another method by which
lice are passed from adult to young birds.

For dispersal and survival the lice must pass from individual to
individual of the same species of bird host. This may take place
during mating, brooding of the young, roosting of gregarious species
and by the use of common dust baths. On the death of the bird
the lice are doomed to extinction unless they can transfer them-
selves quickly to another individual, for the lice soon become torpid
without the warmth of their host. As the bird begins to cool the
lice come to the surface of the feathers and will leave them for any
warm or rough- textured object. This desire to leave the dead and
now unattractive body of their late host probably accounts for the
many recorded cases of "phoresy" (see p. 18) among the Mallophaga.
Chewing lice have frequently been found attached to louse flies (tail-
piece p. 157) and have also been recorded once on a flea, three
times on mosquitoes, once on a Haematobia (a blood-sucking fly), a
dragon-fly, a bumble bee and a butterfly — this last record by Kirby and
Spence (1826) seems to be the earliest mention of phoresy in the Mallo-
phaga. In the first four cases, the lice had attached themselves to
another parasite off the same host; in the last three, the louse had
probably boarded the insect when it had alighted for a few minutes on
the corpse. An interesting case of phoresy was observed in the Shetland
Isles one summer, where most of the starlings were found to be infested
by feather lice and louse flies. One starling examined immediately

FEATHER LICE I37

after death, had seven Hce attached to the inside of the webs of some of
the left wing feathers, and eight in a similar position on the right wing,
making fifteen in all. The bird was wrapped in a piece of cloth and two
hours later immersed in chloroform fumes to kill the ecto-parasites.
When it was shaken out over a piece of white paper, eight of the lice fell
out and one louse-fly {Ornithornyia fringillina) ; the remaining seven lice
were found clinging to the abdomen of the fly. These seven lice must
have attached themselves to the fly after the death of the host, using it
as a lifeboat for escape in the emergency. If the louse-fly in such
circumstances finds another starling, the lice are saved, but as the fly is
less host-specific than the Mallophaga, they must often find themselves
transferred to a different species of bird, on which they die, probably
from starvation — the lifeboat has transported them to a desert island.

Other opportunities for lice to pass to hosts of a different species are
not frequent under natural conditions. The lice of brood parasites
such as the cuckoo have already been discussed. Another normal
association is that between predator and prey, and hawks and owls are
sometimes found harbouring a few lice, which could only have come
from a recently eaten victim (Plate VI). Such stragglers probably do
not survive long. Dust baths may be another method by which lice are
transferred, for where chickens and sparrows use the same dust baths,
the latter on examination have been found with a few specimens of
chicken lice. In captivity and under domestic conditions there are
naturally frequent occasions for lice to pass to new hosts.

Lice do not normally leave the living bird and they are only rarely
found away from their hosts, except in the nest where they have been
seen crawling over the eggs and in the nesting material.

Some of the factors which prevent establishment on a new host, even
if the difficulties of transport are overcome, have already been discussed,
(p. 1 24) . These include the physical structure of the feathers which may
make the movement, clinging, feeding and egg-laying of the louse
difficult or impossible, the chemical composition of the blood and
feathers which may be lethal, and the temperature differences which
may affect the development of the eggs and nymphs of the strange
louse. Apart from these factors, the immigrant louse must face the
competition of the normal louse population already well established
and better adapted to the environment on its own host. Furthermore,
the establishment of an immigrant louse species on a new host naturally
requires the presence of individuals of both sexes or a fertilised female.

138 FLEAS, FLUKES AND CUCKOOS

Establishment on strange hosts must have become progressively
more difficult as the louse became more specialised and more closely
adapted to the feathers and other features of the environment afforded
by the particular kind of bird on which it lived. Furthermore, as the
birds diverged from each other during their evolution the environment
of the lice on difierent groups of birds diverged concurrently. In this
way host specificity becomes more and more extreme, each change
in either the louse or the bird making the interchange of lice more
unlikely.

The actual barriers which stand between a louse and a new host,
including the development of host specificity, have resulted in the
extreme isolation of the populations found on any one host species.
These are analogous to populations of free-living animals found on
oceanic islands. Transference of other species from the mainland or
other islands is difficult and infrequent, and should this occur the
competition from already well established species, not to mention lack
of adaptation to the particular island environment on the part of the
new arrivals, makes survival unlikely. It is generally believed that
isolation favours the acquisition of new characters. If these characters
prevent or discourage interbreeding between the two isolated popula-
tions a new species will result, and the two populations will not re-unite
if break-down of their isolation subsequently enables them to mingle
with one another again. This "speciation by isolation" probably
accounts for the large number of species of Mallophaga now existing.
The fleas, in which isolation of populations is far less complete, have
developed many fewer species. In some genera of Mallophaga para-
sitising one order of birds, each species of bird harbours a distinct species
of louse; in other cases a species of louse may be found on two or more
closely-related birds. Some of these may be distinguished from
each other only by small differences in size, in the characters of the
male genitalia, or in the arrangement of the spines and hairs; females
of closely-related species are often indistinguishable.

General Classification. It is now possible to summarise the evolution-
ary trends which have been responsible for the great number and
diversity of forms found in this group of ecto-parasites. As we have
seen, the Mallophaga are most probably derived from free-living
ancestors which also gave rise to the Psocida or book-lice. The nearest
living relatives of the feather lice are the Anoplura or sucking lice of

FEATHER LICE iqg

which Pediculus humanus, the human louse, is a well-known example. The
sucking lice, which are found only on mammals, feed solely on blood,
their mouth-parts being highly modified for piercing and sucking.
The Mallophaga and the Anoplura are classified as suborders of the
same order — Phthiraptera — thus showing the relationship between the
two groups. The primitive ancestral Mallophaga must have split at an
early period into two stocks which evolved on different lines, and which
gave rise to the two distinct superfamilies, the Amblycera and Ischno-
cera (Plate XXII). The early Mallophaga, especially the Ischnocera,
occupied the different ecological niclaes found on the bodies of their
hosts, and became specialised and adapted for the characters of each
niche. This, as we have seen, meant considerable modifications in
the external morphology (Plates XXI and XXIII), involving
many superficial distinctions, although the characters of the internal
anatomy and basic morphology of the Ischnocera are mostly very
similar. This last fact suggests that evolution of the basic Ischnocera type
was relatively rapid and took place before their occupation of the
different ecological niches, to which they subsequently became adapted.
Possibly the primitive birds had a more uniform feather covering,
somewhat similar to that of the ostriches and rheas, which did not
provide the different ecological niches present in the more recent orders.
This is partly confirmed by the Mallophaga of these present-day primi-
tive birds which present only one generalised type, none being specially
adapted to the neck or wings. The basic similarity of the Ischnocera,
in spite of their superficial differences, makes the classification into
families difhcult, and the present unsatisfactory arrangement will not
be discussed here.

ORDER PHTHIRAPTERA

SUBORDER MALLOPHAGA (chcwing lice) anoplura (sucking lice)

SUPERFAMILY amblycera ischnocera

For scientific purposes the birds are classified or divided into groups
or orders, and those characters which affect the louse, such as the
minute structure of the feathers, are generally uniform throughout the
order. Consequently the lice which occupy an identical ecological

1^0 FLEAS, FLUKES AND CUCKOOS

niche on hosts belonging to one order are generally very similar in
character, and fall naturally into distinct genera. Thus as a rule all the
head lice parasitising one order of birds such as the raptores (Falconi-
formes) belong to one genus {Craspedorhynchus) and all the wing lice
to another {Falcolipeurus) .

As the evolution of the birds lost its initial momentum and slowed
down, the character differences which affected their Mallophaga must
have been gready reduced. The waders, gulls and auks, which together
comprise the order Charadriiformes, show great diversity in habits and
general body form, such as legs, beak, and size, but the environment
they provide for the parasite — for example the physical and chemical
composition of the feathers and blood— is probably constant throughout
the order. Even if lice become isolated on one species of bird, or group
of species, within this order they are not subjected to any violent
change. This results in the development of only small constant distinc-
dons, in other words, specific diflferences. A number of these species
makes up the genus distributed throughout the order. Even when a
group of closely related hosts appear to provide the parasites with an
exactly similar environment, the lice on each host may be disdnct
species, differing in non-adaptive characters — often the male genitaUa
— which have developed as the result of isolation and time.

The isolation of lice within an order of birds has occurred much later
than the isoladon between orders — hence the lice of gulls and plovers
differ from each other less than the Hce of ducks and plovers.

Many birds are parasitised by four or five species each belonging to
a different genus, and in addidon may harbour two or even three
species of one of these genera. These latter species may differ in small
ways only, such as the arrangement of hairs on the abdomen, or by
some character of the male genitalia, or the presence or absence of en-
larged antennae in the male.

This is, of course, a highly over-simplified picture of the process
of evolution in the group. In reahty it has become modified and the
Hnes obscured by various causes which will be further discussed on
pages 142-145, but until we have more information on the distribu-
don, morphology, biology and genetics of the group no definite
conclusions can be reached. However, these tentative suggesdons may
serve some useful purpose in demonstrating the complexity of the many
factors which have influenced the evolution of the Mallophaga. " By
reason of their subtilitv, intricacy, crossing, and interfering with one

FEATHER LICE I4I

another, and the apparent resemblance they have among themselves,
scarce any power of the judgment can unravel and distinguish."

Phylogeny of Host and Parasite

The evolution of the birds, in comparison with many other groups
of animals, is believed to have been rapid. The earliest known bird —
or perhaps feathered reptile would be a better description- is represented
by a fossil {Archaeopteryx) from the Jurassic rocks some 120 million years
old; but by the Upper Eocene, some 60 million years later and between
40 and 70 million years ago, the fossil record shows that most of the
present orders and even families of birds were established. This relatively
rapid divergence and the fundamental changes which took place have
left few traces of the primitive arrangements of bones and muscles,
characters upon which relationships in the vertebrates are mainly
based. This, together with the paucity of the fossil record, due to the
fragile nature of the bones of birds, has left the student of bird evolution
largely groping in the dark. It would be of the utmost value, therefore,
if the present distribution and relationships of the Mallophaga could
throw some light on the phylogeny (or evolutionary relationships) of
their hosts, the birds. The course of evolution in the Mallophaga has
resulted in related bird hosts harbouring related Mallophaga. It has
been shown, for instance, that the head lice of all the waders are closely
related species of one genus. Can we make the reverse deduction and
affirm that the hosts must be related if the parasites are related, and
perhaps convince the ornithologist that relationships between the para-
sites can be a fruitful and reliable source of evidence for relationships
between the hosts ?

The flamingoes (Phoenicopteridae) provide the classical example of
the usefulness of such deductions. In modern classifications, as we have
seen, these birds are usually placed with storks and herons (Ciconii-
formes), more rarely with swans, geese and ducks ( Anseriformes) . The
flamingoes are parasitised by species of three genera of feather lice
[Anatoecus^ Anaticola, and Trinoton) which are found elsewhere only on
the Anseriformes. The species parasitising the Ciconiiformes, on the
other hand, belong to different genera and are quite distinct from
any found on the flamingoes or the Anseriformes. The most likely
explanation of the presence of three duck-infesting genera on the

142 FLEAS, FLUKES AND CUCKOOS

flamingoes is that these genera were already established on an ancient
Anseriformes-stock before it gave rise to the flamingoes on one hand, and
to the modern ducks, geese and swans on the other. This would mean
that the flamingoes are more closely related to the ducks and geese than
to the storks and herons, and, hence, should be included with the
former in the Anseriformes and not in their more usual position with
the Ciconiiformes. The ostrich [Struthio camelus) of South Africa and
the rheas [Rhea americana and Pterocnemia pennata) of South America
provide a similar case. In modern classifications it is assumed that
these birds are not closely related and hence they are placed in
separate orders, the Struthioniformes and the Rheiformes. Both the
ostrich and the rhea, however, have closely related species of a genus
of Mallophaga [Struthiolipeurus) which is found on no other bird. This
strongly suggests that the rheas and ostriches must have shared a com-
mon ancestor, also parasitised by the genus Struthiolipeurus, and that
this genus was in existence in its present form before the separation of
the continents of S. Africa and S. America.

These two examples are instances where the evidence from the
parasites apparently conflicts with the evidence from the anatomy of the
birds. Has the evidence been incorrectly interpreted by the ornitholo-
gist or the parasitologist ? Here we can discuss only how the latter may
have been mistaken, and for this it is necessary to consider the possible
factors which may have influenced and obscured the original evidence,
and thus misled the parasitologist.

Discontinuous distribution. We have already discussed (p. 134) the
discontinuous distribution of certain genera of Mallophaga. If we are
trying to deduce relationships between different birds from the fact that
they are parasitised by the same genus of Mallophaga, it is at once
obvious that genera which show a discontinuous distribution may be
misleading. Passerines and game-birds in this country are both para-
sitised by species of the genus Menacanthus, but this does not suggest a
close relationship between the two orders, for we also find species of this
genus on the tinamous (Tinamiformes) of S. America, the plantain-
eaters (Musophagidae) of Africa, as well as the woodpeckers of this
country, while related genera are found on other orders. This suggests
that Menacanthus was once widely distributed throughout the whole
class of birds, but is now extinct on most orders.

FEATHER LICE I43

Primitive genera. In the superfamily Ischnocera there are some genera
or groups of genera, which have a primitive type of head (Plate XXIIIa)
and which have not become adapted to any particular habitat on the
bird nor to the feather structure characterising any particular group of
birds. Examples of these less specialised genera are found on most of
the orders, and naturally appear more closely related to each other than
to those genera which have become highly specialised. Such primitive
genera cannot, therefore, be used in the consideration of relationships
between birds.

Secondary infestations. It is rare, as we have already seen (p. 135), for
a louse from one bird species to be transferred to another, and if this
does take place, the host specificity of the louse makes establishment on
the new host difficult or impossible. Have there been, nevertheless, cases
in the past where a louse has become established on a new and different
host and there developed into a new and different species ? The answer
is almost certainly in the affirmative. Secondary infestation may ex-
plain the presence of one peculiar louse species found on the British
skuas (Stercorariidae). The skuas are related to the gulls and belong to
the order Gharadriiformes. They are parasitised by species of lice
belonging to four genera found throughout the Gharadriiformes in-
cluding the gulls. In addition, three of the species of skuas which visit
this country are parasitised by a louse belonging to another entirely un-
related genus, which is otherwise peculiar to the petrels (order Pro-
cellariiformes) . This strange distribution can be explained by assuming
that lice from a petrel managed to transfer to a skua, became established
and gradually developed into a new species. Skuas in this country are
known to feed on the dead bodies of at least one petrel, the manx shear-
water, which suggests a possible way in which the original transfer
might have occurred. Because the event has presumably taken place in
relatively recent times it is still possible to deduce what has happened.
The discovery of one species of petrel louse on the skuas does not tempt
us to suggest a relationship between the skuas and the petrels — any more
than some future etymologist would suggest a relationship between
English and Tamil because the word "curry" occurs in both languages.
However, the petrels are further parasitised by a genus which is also
found on the gulls and throughout the Gharadriiformes. This group is
one of the head-lice genera, which tend to become specialised to a
particular host, and are unlikely to be relics of a universal distribution.

144 FLEAS, FLUKES AND CUCKOOS

It may well be that there are certain superficial resemblances between
the external characters of gulls and petrels due to adaptation to life at
sea, which has favoured a certain limited interchange of lice. The
possibility of such secondary infestations — whether ancient or relatively
recent in origin — must always be borne in mind when considering the
distribution of a genus of feather lice in relation to host affinities.

Convergent and parallel evolution. The classification of birds, which is
intended to reflect their true relationship, is based mainly on the
characters of the muscles and skeleton — structures which do not directly
affect the parasite. If two unrelated groups of birds, perhaps in response
to the same environment, developed similar external characters, then
the adaptations to these characters forced on their Mallophaga might
produce in the latter a superficial resemblance to one another even
though they were really not closely related. This type of convergent
evolution in the parasites can suggest false relationships between the
hosts. For example, Pkilopterus, a head louse genus parasitising the
Passeriformes, is mostly very uniform in character. Certain species,
however, have developed a line of thickening on the front margin of the
head, and have a different arrangement of head sutures and of the
struts supporting the mouth-parts. Lice with this type of head have
been found on eleven species of Passeriformes belonging to nine different
families and also on the family Momotidae (the motmots) usually placed
in the order Coraciiformes. Does the similarity of these Mallophaga
suggest that the families of birds on which they are found are more
closely related to each other than to any other of the families of passer-
ines ? There is no evidence of this from ornithological sources, but it
may be that the bird species all have some character in common : the
head feathers of some, at least, of the hosts are hard and shiny, showing
iridescence. The species of the genus Philopterus are sedentary and highly
adapted to the particular feathers on which they move and feed. Any
change in feather structure will tend to affect the front of the head
which is used to push through the plumage, and also the mouth-parts
and their supporting structures used in grasping and feeding. In the
case of these species from the motmots and some of the passerines,
therefore, it seems possible that they have responded with similar
modifications to a similarity of the feathers, possibly a hardening of the
surfaces. The resemblance between these lice is, therefore, due to con-
vergence in response to a similar environment. In such cases it is easy

FEATHER LICE 145

to draw false conclusions concerning the natural relationship of the hosts.
Parallel evolution as we have seen (p. 134) can give rise to a false
impression of close relationship. The occurrence on two groups of birds
of similar, but in fact not closely related, genera naturally does not indi-
cate relationships between the hosts.

Lack of knowledge. The prudent parasitologist will do well also to
admit his ignorance. Ignorance of distribution, biology, ecology,
genetics and morphology accounts for our inability to answer many
questions. At present we are unable to distinguish which of the various
causes may have been responsible in any particular case. Through lack
of morphological knowledge errors may be made in the classification of
the lice themselves and thus any deduction concerning the relationships
of their hosts will be invalidated.

Evidence from other parasites. It is obvious that any supposed relation-
ship between birds which is deduced from the relationship between
their Mallophaga will be greatly strengthened if the case can be
supported by evidence from other parasites. The ornithologist who is
altogether sceptical of the parasitological evidence will nevertheless find
it difficult to explain the presence of closely related species of feather
lice, parasitic worms and mites on two birds which he does not consider
are related. This is the case with the ostrich and rhea. As we have
seen these two birds are now placed in different orders by the ornitholo-
gist. Nevertheless, their feather lice belong to the same genus {Struthioli-
peurus) which is found on no other birds, they are parasitised by closely
related subspecies of the same tapeworm (Houttuynia struthiocameli),
which is not found in other birds, and the same two species of mites
[Paralges pachycnemis and Pterolichus bicaudatus) occur on both hosts.
The presence of these parasites belonging to widely separated classes
cannot be explained away by the theories of discontinuous distribution
or of parallel and convergent evolution; nor is it likely that two birds
separated by the Atlantic Ocean could have become infested with each
other's parasites.

It is necessary for the workers on the various groups of parasites to
co-operate and to present to the ornithologist as complete a picture as
possible of the parasitic fauna of the birds. It is also necessary to empha-
sise which part of the evidence is considered reliable and which may be
misleading. This is particularly important in the case of parasites with

146 FLEAS, FLUKES AND CUCKOOS

intermediate hosts, such as the flukes, which may show a false host
specificity due to the common habitat and diet of their hosts (ethological
specificity, p. 45).

In conclusion it can be said that as a general principle the relation-
ships between the Mallophaga reflect those existing between their hosts.
Birds with a doubtful systematic position cannot be placed on the
evidence of their Mallophaga if only one genus of feather lice is
available from which to draw conclusions, for this may be an ancient
straggler or a relic. If, however, these birds harbour three or more
genera common to the birds of another order this may be taken as
strong presumptive evidence that the hosts in question belong to that
order. The flamingos are a case in point. The ornithologist should
accept the evidence from this source at least as a clue to relationship,
just as he accepts anatomical evidence of bone loss or the arrangement
of a muscle. Alone, any one point will not establish the position of a
bird of doubtful affinities, but the total sum of such evidence from many
sources may be overwhelming. In the future, when the feather Hce as a
group are as well known as the butterflies, the evidence from this
source may be of great significance in the study of the origins, relation-
ships and ancient distribution of various families of birds.

The student of Mallophaga, in this aspect of his work, can be
compared to the palaeontologist. He delves into the past, not by
quarrying in the rocks for fragments of bones, but by studying the
morphology and distribution of these living fossils. As he pieces to-
gether the story of their evolution, he hkewise unfolds the story of the
evolution of the birds.

The Mallophaga of the British Isles

The distribution of the Mallophaga is, in general, a host distribution,
not a geographical one. The jackdaw, whether living in England,
Scotland, Germany or Scandinavia is parasitised by the same species of
hce. The Mallophaga of Britain are, therefore, the Mallophaga of
British birds. For this reason there is little object in fisting the feather
lice of any specific geographical area; attention should be concentrated
on the study of the louse fauna of a group of related birds, for such
groups are the equivalent of the geographical range of free-living
insects. This statement, nevertheless, needs qualification. There does

^n^

9 9

W. H. Pollen

a. Cuclotogaster sp. from partridge, show-
ing primitive type of head

W. H. Pollen
b. Quadraceps sp. from little gull

W''^<

It'. H. Pollen

\V. H. Pollen

c. Halipeurus sp. wing louse from Manx d. Ricinus sp., from meadow-pipit ( x 23)

shearwater ( x 271

PlaU XXIII DIFFERENT TYPES OF FEATHER LICE

{a. — c. Superfamily Ischnocera; d. Superfamily Amblycera)

a. Secondary feather showing eggs ( x 1-4)

J . C. Bradbury

J. G. Bradbury
h. Close-up showing eggs lying between barbs ( x 16)

Plate XXIV EGGS OF WING FEATHER LOUSE

FEATHER LICE 1 47

seem to be in some cases a true geographical distribution superimposed
on the host distribution. A higher percentage of infested individuals
may be found in parts of a bird's range, and certain species of lice seem
to be absent from their host in some localities. The pouch-louse, found in
all the pelicans (Pelecanidae), has been recorded from the related cormor-
ants (Phalacrocoracidae) from the New World and Antarctic species,
but never from those of Africa and Europe.

We have already seen that each bird species supports the repre-
sentatives of a number of genera of feather lice ; some birds may
also harbour two or more species belonging to one genus. The
sanderhng has five, the rook may have six and one of the S.
American tinamous is parasitised by the bewildering number of
twenty-one species belonging to twelve genera and three famihes.
Although many of the species of Mallophaga are found on more than
one kind of bird it follows that there must be a large number of them in
the world. Of these probably less than half have been named, and
many not even collected. The number of species hkely to be found on
the 400 or so birds on the British list can only be estimated within wide
limits, say 500 — 1,000. Again, a number of these still has no valid
scientific name ; even two of the Hce from the common rook are un-
described and consequently are still nameless. There are few specialists
working on the group, for it is of no medical and of Kttle economic
importance. Hidden as they are in the plumage of the bird, feather
hce do not attract the immediate attention of the naturalist and few
people even know that they exist. Moreover, they are difficult to
collect, and when collected must first be treated and mounted on
glass slides and then examined under the microscope. Species are
distinguished from each other mainly by the details of the male
genitaha, which for microscopic study must be dissected and mounted
separately. When the louse is ready for identification it is first
necessary to know whether it has already been described or named.
This is not easy. The early authors — the first figures were published in
1668 by the great Itahan biologist Redi— did not realise the importance
of the small characters necessary for separating species, so that their
descriptions and figures can only serve to identify the genus, and that
sometimes doubtfully. Nor did the early authors always name the host
from which they took the louse, or they recorded it from three hosts,
which are now known to harbour three distinct species office. Lastly, the
systematics of the Mallophaga are cursed by records of straggling feather

FFC— L

1^8 FLEAS, FLUKES AND CUCKOOS

lice. A "new" species is described from a hawk, which in reaUty is a
straggler from a wader, shot at the same time and put in the same
collecting bag. If the original description is inadequate a .^pecies of wader
louse appears in the literature, the host of which may never be found,
and which naturally baffles the expert. It is hke expecting an ornitho-
logist to identify an exotic finch from an inadequate description
coupled with the information that it was obtained in England — where
its presence was solely due to an aviary door having been left open.
Thus, there is a great deal of work to be done in the interpretation of
the old names and the accurate re-description of these species, before
many of the British Mallophaga can be named or descriptions of new

species made.

The general classification of the Mallophaga has already been out-
lined (p. 139), and we can now discuss, in rather more detail, how this
can be applied to the feather hce found on British birds. It must be
emphasised that, for the reasons already considered, the present classi-
fication is far from satisfactory and will need drastic modification as our
knowledge of the group becomes more extensive.

As we have seen, the suborder of the Mallophaga is divided into two
superfamilies : the Amblycera and Ischnocera.

Reference has been made in the preceding pages to these two
superfamilies, and it will have become apparent that they show
considerable differences in habit and form (Plate XXII). The Ambly-
cera, as we have seen, show less diversity in structure and are divided
into a smaller number of families and genera. There are three families
of Amblycera found on British birds, the Laemobothriidae, Ricinidae
and Menoponidae.

The Laemobothriidae are represented in this country by one genus,
Laemobothrion, found on hawks. This genus contains the largest of the
Mallophaga, and at the present time has only been taken from the
kestrel although from non-British records it is known to parasitise other
hawks on the British list.

The Ricinidae is also represented in this country by only one genus,
Ricinus (Plate XXIII) restricted to passerine birds of which the robin
and the chaffinch are the common hosts. It is the largest of the species
found on this group of birds, and the comparatively large shiny white
eggs can often be seen in great numbers on the feathers of the neck and

throat.

The Menoponidae (Plate XXIIa) contains a number of genera.

FEATHER LICE I49

examples of which are found on all the British orders of birds. These
genera do not differ greatly from each other and for the present are
contained in the one family.

The Ischnocera, as we have already seen, are more specialised and
adapted to particular environments, and hence show a greater diversity
in their structure (Plates XXI and XXIII, a-c). This fact is reflected
in their classification by the larger number of families and genera into
which they are divided. The species found on British birds are contained
in forty-three genera. No attempt will be made to give the characters
of the famiHes and genera, which is a detailed and specialised subject
outside the scope of this book. The large number and anonymous state
of the Mallophaga make it impossible to do more than mention some
of the more interesting ones found on British birds.

Passeriformes
Genera of Mallophaga recorded in Britain: Colpocephalunij Myrsidea,
MenacanthuSj Ricinus (Amblycera); Briielia, Sturnidoecus, Penenmnns,

Philopterus (Ischnocera).

In this country the passerine birds may be parasitised by species of
any of these eight genera. Five others have been recorded from this
order in the New World. The rook harbours five of these genera, which
in Britain is the maximum for any one species of passerine, but they are
not necessarily all found together on one individual. These lice illustrate
the rather curious fact that the size of the birds in an order has no
bearing on the number of different genera which may be found upon
them. The Passeriformes have thirteen genera, the Struthioniformes
(ostriches) only one. The passerine birds also illustrate another un-
expected fact, namely that the genera containing the largest lice are not
necessarily found on the largest hosts, despite the fact that there is often
a correlation between the size of host and louse within a given genus.
In Ricinus (Plate XXIII), a genus confined to the Passeriformes, the
largest females may measure 4.5 mm. (about one-fifth of an inch) in
length. Feather lice of a comparable size are found, amongst British
birds, only on hawks, ducks, and fulmars, all of which are considerably
larger than the robin and the finches which are the most usual hosts of
Ricinus in tliis country.

150 fleas, flukes and cuckoos

Apodiformes
Genera of Mallophaga recorded in Britain : Dennyus, Eureum

( Amblycera) .

The swifts are the only order of birds known from which no member
of the superfamily Ischnocera has been recorded. They harbour species
of two related genera of Amblycera, which are unlike those found on
any other order of birds and confirm the isolated position of the swifts
within the class Aves.

Caprimulgiformes
Genus of Mallophaga recorded in Britain : Mulcticola (Ischnocera).

The British nightjar has only one species of Mallophaga, a wing
louse. Other kinds of nightjars found in the New World are, however,
also parasitised by a head louse.

Coraciiformes
Genera recorded from the order in Britain : Alcedoecus, Alcedqff'uia
(Ischnocera) from kingfishers; Meropoecus^ Briielia (Ischnocera) from
the bee-eater; Menacanthus{Amb\ycQY2i), Upupicola {Ischnocera.) from
the hoopoe. There are no records from British-taken rollers, but
one genus Capraiella (Ischnocera) has been found on rollers from

the continent of Europe.

This order is represented in Britain by one resident, the kingfisher
and three vagrants, the bee-eater, the hoopoe and the roller. The
kingfisher is parasitised by two closely related genera of Ischnocera but
lacks Amblycera; these two genera are not closely related to those found
on any other bird. The kingfisher is a case where the Mallophaga
throw no light on the relationships of the host, but the feather lice
found on the three vagrants mentioned above suggest that they are
related to the Passeriformes.

Piciformes
Genera of Mallophaga recorded in Britain : Menacanthus (Ambly-
cera); Briielia, Penenirmus (Ischnocera).

The species of Mallophaga found on the British woodpeckers
belong to genera also found on the passerine birds, which tends to

FEATHER LICE I5I

support Lowe's theory that the woodpecker should not be placed in a
separate order. It has been suggested that if the habit of anting by
birds helps to rid them of lice, the green woodpecker, as a frequent
visitor to ants' nests, should be less heavily parasitised than the other
woodpeckers ; this has not been found to be the case.

CUGULIFORMES

Genera of Mallophaga recorded in Britain : Cuculiphilus (Ambly-

cera); Cuculicola, Cuculoecus (Ischnocera).

The method of dispersal and other interesting points connected with
the lice of the cuckoo, a brood parasite, have already been discussed.
Another curious fact is that the Mallophaga of the cuckoo — superficially
so like a hawk and also mobbed by other birds — belong to genera which
are either the same or apparently closely related to those found on the
hawks. At the present time we cannot say what the significance oi
this fact may be, but when considering the Mallophaga only, the
parasitologist is reminded of the words of Pliny : " The cuckoo seems
to be but another form of hawk."

Strigiformes
Genera of Mallophaga recorded in Britain : Colpocephalwn,
Kurodaia (Amblycera) ; Strigiphilus (Ischnocera).

The members of this order in Great Briatin are parasitised by only
three genera of lice, one belonging to the Ischnocera, and two to the
Amblycera. Owls, like hawks, may also have a temporary population
of lice which have straggled from their prey. A short-eared owl from
S. Uist was infested with five specimens of lice belonging to three
different genera which must have come from a wader it had recently
killed.

Falconiformes

Genera of Mallophaga recorded in Britain : Colpocephalunif

Kurodaidj Laemobothrion (Amblycera); Degeeriella, Falcolipeurus,

Craspedorrhynchus (Ischnocera) .

The British hawks are usually parasitised by two species of Ischno-
cera, one a typical head louse, the other belonging to a more primitive,

ir2 FLEAS, FLUKES AND CUCKOOS

unspecialised genus; a third genus [Falcolipeurus) has only been taken
from the golden eagle. The Amblycera are represented by three genera,
and there is a fourth which has not been taken from British birds of
prey. Two of these genera illustrate the kind of anomalous distribution
which may bring the student of Mallophaga into conflict with the
ornithologist, since one of them is also found on the owls, the other, as
we have already seen, on the cuckoos.

In modern classifications the Raptores, owls and cuckoos are not
considered to be related in any way.

CiCONIIFORMES

Genera of Mallophaga recorded in Britain : Colpocephalum,
Ciconiphilus, Ardeiphilus (Amblycera) ; Ardeicola, Neophilopterus

(Ischnocera).

The two members of this order resident in Britain, the heron and
the bittern, each have two species of lice. The plumage of the heron
seems to offer no attraction for the Mallophaga, for it is a bird which
seldom supports a large populadon and many individuals are altogether
louseless. A head louse is absent, although one is present on other
members of the order such as the spoonbill. One wing louse is recorded
—a species that is flabby and pale in colour, due perhaps to the soft
texture and light colour of the heron's plumage— and one member of
the Amblycera. On the other hand the white stork, a vagrant to
Britain, harbours species belonging to no less than four genera of feather
lice.

Anseriformes

Genera recorded in Britain : Ciconiphilus, Holomenoporiy Jrinoion

(Amblycera); Anatoecus, Anaticola, Ornithobius (Ischnocera).

The ducks and geese in Britain are usually parasitised by four
genera : one short and round in form and adapted to life on the head
and neck, one flattened and elongate and living on the back and wings,
while the other two genera belong to the Amblycera. One of these
{Trinoton, Plate XXII) seems to be the fastest runner of all lice. It
probably roams through the plumage and requires speed, not only to
escape the bill during preening, but to be able to get well into the
plumage in the case of a crash dive by the duck. The swans have, in

FEATHERLICE 1 53

addition, species of another rather large genus {Omithobius). It is
interesting that this louse, as well as the one found on the wings, is pale
in colour, as if to match the white plumage of its hosts. The head
species has retained the usual brown colour characteristic of the
members of the genus {Anatoecus) which parasitises all the Anseriformes.

Pelecaniformes

Genera of Mallophaga recorded in Britain : Eidmanniella (Ambly-

cera); Pectinopygus (Ischnocera).

The cormorant, the shag and the gannet each have species of only-
two genera, one belonging to the superfamily Amblycera and one to the
Ischnocera (Plate XXIIb). It is interesting that there is no louse
adapted to the head niche, and it may be that the short feathers of the
head do not provide sufficient covering for the lice of birds which
spend some time under water. The grebes and divers also have no
head lice.

Procellariiformes
Genera of Mallophaga recorded in Britain : Austromenopon,
Ancistrona (Amblycera) ; Halipeurus, PerineuSj Trabeculus, Saemunds-

sonia (Ischnocera).

Mallophaga have been recorded from three of the resident British
petrels — the storm-petrel, the manx shearwater (Plate XXIIIc) and the
fulmar. The manx shearwater has five species of Mallophaga, one of
which belongs to a genus of large species {Ancistrona). Species of this
Amblyceran genus on related shearwaters {Puffinus) have been found
with eggs and adults of a parasitic mite attached to their abdomens.
The only other record of this mite {Myialgopsis trinotoni) is from the genus
( Trinoton) found on ducks, geese and swans — the species of which are
also among the largest of the Mallophaga.

PODICIPITIFORMES AND COLYMBIFORMES

Genera of Mallophaga recorded from the grebes in Britain :
Pseudomenopon (Amblycera); Aquanirmus (Ischnocera). Genus
recorded from the divers in Britain : Craspedonirmus (Ischnocera).

The British grebes and divers each have one characteristic genus of
Ischnocera. These genera do not appear to be related to each other nor

I. "3^ Fl.KAS, FLUKES AND CUCKOOS

to any other genus —which reflects the bcHef that the grebes and divers
themselves are not closely related to each other, nor to any other living
order of birds. This wholly supports the evidence obtained from a study
of their tapeworms (see p. 193).

COLUMBIFORMES
Genera of Mallophaga recorded in Britain : Colpocephalum,
Hohorstiella (Amblycera); Campanuloles, Coluceras, Colu?nbicola

(Ischnocera).

The British pigeons may harbour species of hce belonging to five
genera, and one of these (Campanulotes) illustrates the correlation between
louse size and the size of the host (further discussed below). Thus the
three species of this genus found on the wood-pigeon, the stock-dove and
the rock-dove are very similar, but that from the wood-pigeon is
noticeably larger than those from the other two. Further, if a large
number of specimens from the two latter hosts are measured, those from
the rock-dove are found, on the average, to be smaller. The lice may,
therefore, reflect some hitherto unrecorded differences in the size of
the host.

Charadriiformes

Genera of Mallophaga recorded in Britain : Actornithophilus ,

Austromenopon (Amblycera); Rhynonirmus, Lunaceps, Carduiceps,

Cummingsiella, Quadraceps, Saemundssonia (Ischnocera).

The members of this order, which contains the waders, gulls and
auks, may be parasitised by species of any of eight genera of lice. The
most interesting louse found on the waders is the quill-louse {Actorni-
thophilus patellatus, Plate lb) of the curlew. The information about this
species is still incomplete, but from records of curlews examined in this
country it is known that 44 per cent, have specimens of the quill-louse
on their bodies, and of this 44 per cent., over half have holes in the
shafts of the wing feathers. There is a remarkable symmetry in the
position of the holes, and it is usual for the same quills to be attacked in
both wings. If the seventh to the eleventh primaries are entered in the
right wing, the seventh to the eleventh will also be entered in the left.
The primaries on each side are also attacked in the same order : if the
sixth to the ninth on the right wing have completed holes, with the
beginning of a hole on the tenth, this will often be repeated in the

FEATHER LICE 1 55

left wing. There is also symmetry in the position of the two holes on the
opposite wings. Thus, in one curlew examined, the hole in the seventh
primary on each side was 51 millimetres from the base, in the eighth
primary 57, in the ninth 54, and in the tenth 57 millimetres. Some of
the feathers may have more than one hole. The louse can hardly be
credited with the human passion for symmetry, nor is it at all likely that
specimens on one side of the bird know what transpires on the other.
The answer is most probably that there is a correlation in moulting
time between the two wings and that the louse attacks the feather at the
earhest moment after its maturity and at the easiest place for boring
the hole. The Mallophaga seem to feed on the feather caps left by the
withdrawing papilla. The eggs, as in the case of the quill mite, are laid
in spiral curves within the shaft; the young develop within the quill and
again like the mite leave the quill before the moult is due. A great deal
more information on the biology of this louse is needed, including such
details as the condition both of the feathers attacked and those not
utihsed, and the time of year when the unhatched eggs and nymph al
stages are found within the shafts. Anyone who has the opportunity of
handling a dead curlew should look out for such points and record
them. This louse has been taken from the wings of the curlew, both in
this country and America, but from no other wader; all birds, especially
waders, should be examined for the minute holes on the shafts of the
primaries and secondaries which are made by the quill lice.

The head lice of three of the British terns are a good illustration of
the frequent correlation found between louse size and host size. The
smallest louse is found on the little tern, the largest on the sandwich tern
and a louse intermediate in size on the intermediate sized host, the
common tern. What accounts for this correlation in size ? There
may be a close relationship between size of feather parts and size of
bird, and this might directly affect the dimensions of the louse. At the
present time Httle is known about the differences in feather structure of
related species of birds.

Ralliformes

Genera of Mallophaga recorded in Britain Pseudomenopon

(Amblycera); Rallicola, Incidifrons, Fulicqffula (Ischnocera).

The British rails may be parasitised by three or four species of lice.
The large Eulaemobothrion has never been found on any of the British

156 FLEAS, FLUKES AND CUCKOOS

rails, but has been taken from the coot in Morocco, India and the U.S.A.
the moorhen in Uganda and the Sudan. This is an example of geo-
graphical as opposed to the more usual host distribution of a parasite.

Galliformes

Genera of Mallophaga recorded in Britain : Menacanthus, Amyr-

sidea, Menopon (Amblycera); Cuclotogaster^ Lipeurus, Oxylipeurus^

LagopoecuSj Goniocotes, Goniodes (Ischnocera).

The game-birds of Britain harbour species of nine different genera
of Mallophaga. Not all of these are found on any one of the game-
birds, five being the greatest number of species recorded from a single
host. Pheasants, because they are frequently reared under hens, may be
infested with lice of their foster-parents. These birds, introduced into
Britain probably by the Romans, harbour exactly the same species of
Mallophaga as the wild pheasants of Afghanistan — a case where the
parasite is unaffected by the geographical locality in which the host is
found. The same may be said about t^e domestic hen which harbours
a similar species of Goniodes to the wild jungle fowl. The fleas, on the
other hand, which infect game birds in Britain, are species which
they have acquired in temperate climates.

Conclusion

It will have become evident while reading these pages that our
ignorance of the feather lice is abysmal. What we do not know far
exceeds what we know. Their biology particularly requires investiga-
tion. Lice cannot be kept alive off the host except in an incubator at
the right temperature and humidity, and a supply of fresh feathers of the
appropriate host must be available. Providing these conditions can be
fulfilled the solution of a large number of problems could be attempted.
These relate to life history, food preferences, host specificity, and the
louse in relation to its environment in general. More information is
also needed concerning the morphology, distribution and the particular
habitats of the lice on any one bird, distribution of lice on the same host
species in different geographical areas, and distribution on the different
host species within one order of birds. The student who intends working

FEATHER LICE

157

on the Mallophaga should take warning that he will be tried almost
beyond endurance by the paradoxes and complexities which beset his
subject but he will also find, in the dual and inter-related aspect of
insect and bird, an infinite fascination.

Phoresy; louse-fly transporting feather lice (x 10)

PART THREE

INTRODUCTION

If I should count them they are more in
number than the sands.

Psalm 139:18

IT WOULD have been most satisfactory if, in Part III, we could
have supplied a complete check list of the parasites of British birds.
Such compilations make dull reading but from the practical, scientific
angle would provide a valuable and badly needed piece of work. The
chief bar to drawing up a check list of this type is the vast numbers of
scattered records of parasites recorded abroad from birds on the British
list, coupled with the paucity of genuine records from birds in Britain.
A list restricted to the latter parasites would be altogether misleading
and practically valueless, even if the species likely to occur in this
country were included, whereas the compilation of the former list
represents a herculean task few would feel inclined to undertake —
certainly not the authors.

The following chapters are, therefore, intended to give the reader a
rapid survey of the main groups of bird parasites in Britain and to point
the way to further ecological and systematic work, and, in particular, to
emphasize the need for further collecting and the accurate identification
of specimens.

158

CHAPTER 9

PROTOZOA

There is nothing funny in the thought that even man, who
was made in the image of God, bears about in his vital organs
various forms of loathsome creatures, which riot on his fluids
and consume the very substance of his tissues.

Philip Henry Gosse

ANIMALS which perform all the functions of life within the compass of
a single cell outnumber all the other animals by a million to one.
These single-celled organisms, which are known as Protozoa (Fig. 2),
vary considerably in size but the largest are only just visible to the
naked eye. The simplest forms like amoeba consist of a blob of proto-
plasm containing a nucleus. In a fluid medium they sometimes
assume a spherical form and under the microscope each is somewhat
reminiscent of a fried egg — although the nucleus is colourless, not
yellow like the egg yolk. In some of the parasitic forms, such as the
Coccidia, the body has a spherical or ovoid shape which lies motionless
within the cytoplasm of the host's cells. On the other hand many types
which live in lymph or blood and other body fluids vary considerably
in appearance and structure. They are endowed with the power of
active movement like the free-living Protozoa which swarm in water
and damp situations.

It is generally believed that the parasitic forms are derived from free-
living ancestors, and as almost every higher animal harbours one or
more species of parasitic, commensal or symbiotic Protozoa, the number
of dependent forms is large. Although only single-celled organisms,
they display many of the adaptations to the parasitic mode of life which
are found in multi-cellular animals. Thus, in some forms special organs
of attachment are developed. A good example of this type of structure
is found in the sucking disc o^Giardia (Fig. 2, g & h) — flagellate which

159

l60 FLEAS, FLUKES AND CUCKOOS

attaches itself firmly to the surface of the intestinal cells of vertebrates,
including birds such as herons, shrikes and avocets. In certain groups
the mouth (cytostome) is frequently missing although this organ is present
in related free-living forms. Cyst formation is also characteristic of
parasitic Protozoa, such as Eimeria from the grouse. Cysts provide
the chief means of transference from host to host, since they protect the
enclosed parasite against the influence of the external environment and
resist the action of the digestive juices of the stomach. These properties
enable the protozoon to gain access to the internal organs of the bird
when swallowed with food and water. An enhanced power of reproduc-
tion involving multiple fission instead of the more usual binary fission
is also a typical feature of the parasitic forms. Complicated life-cycles,
with alternating vertebrate and invertebrate hosts, are found in many
Sporozoa and Flagellata from birds. The development of host specifi-
city and increased virulence are also characteristic of numbers of these
organisms — two phenomena which have been considered in previous
chapters. The parasitic Protozoa of birds (Fig. 2) belong to the three
classes, Sporozoa, Mastigophora and Rhizopoda, of which by far
the most important types are those grouped in the Class Sporozoa.

Class Sporozoa

The Sporozoa are exclusively parasite and live and feed in the cells
and body fluids of other animals. In the absence of a mouth the food
— which is in solution — passes into the body in liquid form and is
absorbed by osmosis. The proteid which is in solution is absorbed in
liquid form. During much of their life-cycle Sporozoa lack organs of
locomotion. They are also characterised by a highly specialised type
of reproduction. At some stage of their development they produce
cysts (oocysts) within which the infective forms called sporozoites are
found. In the Coccidia these are carried to new hosts within this
protective envelope.

The life-cyle is complicated, with alternating sexual and asexual
phases. In the asexual phase, instead of simple division into two
separate individuals the nucleus of the growing parasite, known as the
trophozoite, divides repeatedly. Each resulting nucleus becomes
surrounded by a portion of the cytoplasm, and the body of the parasite,
now known as a schizont, breaks up into daughter individuals. The

PROTOZOA l6l

number of these daughter individuals corresponds to the number of
nuclei present. This process is known as schizogony.

An alternation of hosts frequently occurs, and in such cases one
stage of the life-cycle may be passed in an invertebrate and another in
a vertebrate animal.

Order Cocgidia

In temperate climates Coccidia cause a greater loss to domestic
poultry, pigeons and g^me birds than any other group of Protozoa.
They are also common parasites of wild birds. Shipley pointed out
that the name is somewhat misleading since the public are apt to think
of a Coccidium as a bacterium or coccus^ whereas it no more resembles
this organism than a crocodile resembles a crocus. The best known
family is the Eimeridae (Fig. 2, a) which occurs in birds, mammals,
reptiles, amphibians, fish and arthropods. The whole of the growth
period of these parasites takes place within the cytoplasm of a host cell.
The oocysts are discharged in the droppings of infected birds, and may
contaminate food and water. If ingested by another bird while eating
or drinking, the oocysts pass into the duodenum where their thick
resistant wall is dissolved and the sporocysts are liberated. Each of
these sporocysts in turn sets free two active motile sporozoites which
bore into cells lining the intestine. Here they grow at the expense of
the host tissue. ^Vithin these epithelial cells, multiplication by schi-
zogony occurs repeatedly. The daughter individuals known as mero-
zoites eventually escape into the lumen of the intestine and from there
invade new host-cells. After several of these asexual cycles the resulting
merozoites become differentiated into ovoid macrogametes (female
cells) and flagellated microgametes (male cells). Each type develops in
a separate cell of the host. Copulation and fertilisation take place by a
liberated male cell penetrating a female cell; a resistant wall is formed
round the fertilised cell or zygote which now becomes an oocyst and
bursts out once again into the lumen of the intestine. It is, however,
incapable of further development until it is voided with the bird's
faeces. Conditions in the outside world are favourable and after some
time the single cell within the oocyst divides into two or four spores
(sporocysts). The oocysts have then reached the so-called infective
stage and if swallowed, are capable of infecting another host.

Fig. 2
Different types of parasitic Protozoa (adapted from Wenyon)
a., Eimeria avium, class Sporozoa, order^Coccidia^ (x 1300); b., Leucocyto-
zoon sp., class Sporozoa, order^Haemosporidia (x 2000); c, Haemoproteus
sp., class Sporozoa, order Haemosporidia (x 2000) ; d., Trichoinonas
eberthiy class Mastigophora (Flagellata), order Protomonadida (x 4100)*;
e., Chilomastix gallinarum, class Mastigophora (Flagellata), order
Protomonadida (x 4100) ;/., Eutrichomastix gallinarum, class Mastigophora
(Flagellata), order Protomonadida (x 4100); g., Giardia intestinalis,
ventral aspect, class Mastigophora, (Flagellate), order Diplomonadida
(x 5100); h., Giardia intestinalis, lateral aspect, class Mastigophora
(Flagellata), order Diplomonadida (x 5100); f., Entamoeba sp., class

Rhizopoda, (x 2000)
* {Notil a drawing of Trypanosoma will be found at the end of Chapter 9)

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PROTOZOA 163

The usual sites of infection of Eimeridae are the cells lining the
intestines although occasionally they are found in other organs. Heavy
infestations may cause extensive destruction of the epithelium, which,
in turn results in inflammation and bleeding and the ultimate death
of the host. In small numbers they appear to do little damage
and many birds which harbour Coccidia are apparently in perfect
health.

The two most familiar genera from birds are Eimeria and Isospora.
The latter is found principally in perching birds and is recorded from
various passerines, and also from kingfishers (Coraciiformes), hawks
(Falconiformes), woodpeckers (Piciformes), owls (Strigiformes) and
cuckoos (Cuculiformes) ; 127 species are known to be hosts in the United
States alone. The incidence of infection is also very high — often an
entire population is affected. Eimeria, on the other hand, parasitises the
more primitive orders such as geese ( Anseriformes) , cranes, coots and
moorhens (Gruiformes) , pigeons (Columbiformes), cormorants (Pele-
caniformes) and game birds (Galliformes). Both genera are said to
infect plovers (Charadriiformes) but this record requires corroboration.
Owing to the fact that Eimeria is a pest in farmyards while Isospora does
not attack poultry, the latter escapes attention except from the specialist.
The various species are said to be strictly host-specific, that is to say,
they are peculiar to one sort of bird only. At the same time seven
species of J^fmmfl are recorded from the domestic fowl alone and three
from geese. Some authorities regard the whole lot as varieties of one
species E. avium, which in Britain was first reported from wild birds, in
the grouse (Fig. 2ja). The largest number of victims are found among
chicks under six weeks of age. Altogether young birds are more suscep-
tible than adults. After an infection has been present for some time in
an individual bird, schizogony gradually decreases and only male and
female gametes are produced by the parasite. This leads to the forma-
tion of oocysts which pass out of the body and thus infection gradually
ceases. The cause of this change is not really known, but \\e can hazard
the guess that it is due partly at any rate, to changes in the blood serum
of the host, or acquired immunity.

Eimeria does not need an intermediate host in order to complete its
development and birds can be infected directly by ingesting oocysts.
The spread of the parasite may be assisted by flies, which act as transport
hosts. These insects, both in the larval and adult stages, ingest the
oocysts along with the faeces of the birds, on which they feed. They

FFC— M

164 FLEAS, FLUKES AND CUCKOOS

pass unchanged and unharmed through the ahmentary canal. In this
way, the oocysts arc widely dispersed and they are often ingested by a
bird which catches and eats the fly.

Several workers have claimed that the oocysts appear in the faeces
of infected birds at definite times of the day, between 3 and 8 p.m. for
Isospora and 3 and 9 p.m. for Eimeria. The metabolism of the parasite
would therefore appear to be closely Hnked to the host and the
voiding of oocysts at definite times may be regulated by the bird's
responses to light and dark.

The genera Eimeria and Isospora present an interesting problem in
evolution of host and parasite. Some time in the remote history of
birds the ancestors of these Protozoa parted company. It is interesdng
to follow their development in tne various orders of birds and to see if
other parasites show a similar divergence among the groups in question.

Order Haemosporidia

" Of all the human diseases," wrote Chandler in 1946, "there is
none which is of more importance in the world to-day than malaria.
It has been estimated to be the direct cause of over one-half the entire
mortality of the human race." Man, however, is only susceptible to
one genus of the family Plasmodidae, while birds fall victim to all
three. It is difficult in the present state of our knowledge to estimate
the damage inflicted on populations of wild birds by these parasites.
Judging from observations made on canaries and other species kept in
captivity, and domestic poultry such as ducks and turkeys, the harmful
eflfects must be considerable, even if the mortality rate is not high.

One of the most extraordinary facts in the whole field of bird
parasitology is the lack of research into true malaria [Plasmodium) in
British wild birds. This seems even more peculiar when it is realised
that the transmission of the malaria parasite was first demonstrated by
Ross using wild birds in India. The actual species concerned were a
crow {Corvus splendens), two pigeons, four larks {Calandrella dukhmen-
sis) and six sparrows {Passer domesticus indicus). Moreover, one of
the most effective modern therapeutic drugs, paludrine, was discovered
in this country; canaries and chickens were used for the experiments
concerned. The fact remains that except for a record made over thirty
years ago by Coles, we should not know for certain if true malaria existed
in British wild birds. It is safe to assume that it is not uncommon, for
avian plasmodia undoubtedly occur in every part of the world where

PROTOZOA 165

both birds and mosquitoes are found. After considering all the available
data, Hewitt calculated that the mean rate of infection for all birds is
about 5 per cent. In Germany and Italy the figures are between 4.4
and 4.8. per cent., but in California they rise to 18 and 19 per cent.
Passerines are more susceptible than other birds but a wide range of
hosts — over 200 species — is recorded. These include about 40 on the
British fist such as the great tit, white wagtail, swallow, nightjar and
various finches, buntings, thrushes, warblers, larks, shrikes and so
forth. About twelve species of bird Plasmodium are now recognised
although many have been described several times over in error, so that
the literature is cluttered up with invalid names. Probably not more
than four or five can be expected to occur in Britain. The insect vectors
are mosquitoes, of which by far the most important is the house-gnat
{Culex pipiens) , the commonest of all British mosquitoes. Certain other
species found in this country such as Aedes geniculatus and Theobaldia
annulata are also known to be carriers of the disease.

The Life-cycle of Plasmodium relictum
Various species oi Plasmodium parasitise mammals, birds and reptiles
but the sexual stage of the life history is always passed in insects. The
cycle of the malaria parasite is extremely compHcated and the organism
passes through a constant series of changes of form. P. relictum (formerly
known as P. praecox) was the species with which Ross carried out his
famous experiments. It is common in birds found in tropical and sub-
tropical countries, but to a lesser degree it also occurs in temperate
cHmates and has been recorded from North America, and in Europe
from France, Germany, Austria, Switzerland, Italy and Russia. Some
authorities (see Appendix : Hewitt, Wenyon) assume that the un-
named Plasmodium which Coles recorded from three song-thrushes and
a blackbird in the Bournemouth district of England refers to this species.
The life-cycle (Fig. 3) in the vertebrate host commences when the
sporozoites in the saliva of the mosquito are introduced into the bird
during the process of blood-sucking. The sporozoites at this stage are
minute active worm-like vermicules and, on entering the blood stream,
they are taken up by leucocytes or endothelial cells of different organs,
in which they assume a spherical form and multiply by schizogony.
After several generations of so-called exoerythrocytic schizogony, the
merozoites enter the circulatory system and invade the red blood
corpuscles in which their subsequent development takes place. Once

Fig. 3

Life -cycle o^ Plasmodium falciparum in man and mosquito (adapted from

Wenyon and Brumpt) . The cycle of P. relictum is similar.

PROTOZOA 167

within a red blood cell the merozoite becomes rounded off as a small
mass of protoplasm with a single nucleus, and begins to grow at the ex-
pense of the blood corpuscle. The parasite absorbs haemoglobin and
this is transformed into a pigment consisting of haematin which appears
in the cytoplasm of the parasite as characteristic black or brown
granules. These granules are also found in infections of the allied genus
Haemoproteus but not Leucocytozoon. After a few days of growth the para-
site multiplies by schizogony, giving rise to merozoites, the number of
which varies in different species. These burst out of the blood corpuscle,
which is entirely destroyed, and escape into the plasma of the bird.
Here each merozoite attaches itself to a healthy blood corpuscle and
actively forces its way in. Growth follows and schizogony is repeated
all over again. The periodical attacks of fever, so characteristic of
malaria, occur when the corpuscles are ruptured by the escaping para-
sites and poisonous substances are liberated in the blood stream.

After several generations of merozoites have been produced a
striking change occurs. The merozoites develop into gametocytes
instead of schizonts which remain within the red blood corpuscles until
they are ingested by a mosquito feeding upon the blood of the bird.
Even at this stage it is possible to distinguish between the male and
female gametocytes. In the former the protoplasm stains faintly and
the nucleus is large and diffuse, while in the latter the cytoplasm stains
deeply and the nucleus is small.

On entering the stomach of the mosquito (Fig. 3) the gametocytes,
apparently affected by the change of temperature, burst out of the
restraining membrane of the blood corpuscles. Long thin processes are
then formed from the surface of the male cell (microgametocyte) which
lash about continuously. These are the microgametes, which break
loose at intervals and swim about among the corpuscles in the stomach
of the mosquito. Meanwhile the liberated female cell (macrogameto-
cyte) remains as a more or less motionless sphere with the nucleus dis-
placed somewhat towards the surface of the cell. When a microgamete
comes near, it quickly penetrates the macrogamete and its nucleus
unites with that of the female cell. The spherical zygote resulting from
fertilisation rests for a while and then begins to elongate until it assumes
a wormlike form. It then makes its way through the contents of the
stomach by a gliding and bending motion until it reaches the epithelial
lining of the gut. Here it penetrates between the cells and finally comes
to rest under the elastic membrane which covers the outer surface of the

l68 FLEAS, FLUKES AND CUCKOOS

Stomach. Afterwards the zygote becomes surrounded by a membrane
partly secreted by the tissue of the host and partly by the parasite itself.
The Plasmodium, which at this stage is kno\vn as an oocyst, continues to
grow and tlie nucleus multiplies by schizogony thus giving rise to
numerous minute daughter nuclei. Then the cytoplasm begins to
break up and form finger-like processes into each of which a nucleus
passes. In this way numerous spindle-shaped sporozoites are formed
which eventually break a\vay from their point of attachment and remain
as a tangled mass within each oocyst. Sometimes as many as 30 or 40
such oocysts, each containing up to 10,000 sporozoites, are found
beading the surface of a gnat's stomach — all in different stages of
development, \\lien ripe the oocyst bursts, liberating the mass of sporo-
zoites in the body caN-ity of the mosquito. These pointed, spindle-
shaped cells move about by waves of peristaltic contraction and by a
gliding motion, by means of which they insinuate themselves into every
organ of the mosquito's body. Large numbers reach the sahvar)- glands
and pass up the duct \\-ith the saliva. During tlie insect's next blood
meal they are injected into the blood stream of the bird and the asexual
cycle begins once again.

In recent vears some extremelv interestins; ^vork has been carried
out by James and Tate in England, and by Huff in the U.S.A., using
the fowl malaria parasite {Plasmodium gallinaceum) . They have demon-
strated that the initial asexual cycle in the bird is passed in the white
blood corpuscles and in the endothelial cells of the spleen, heart and
brain. This exoer\"throcytic development is follo^\"ed by invasion of the
red blood corpuscles in which the parasite continues to multiply by
schizogony. These discoveries paved the way to similar discoveries
made by Shortt relating to the human malarial parasite and have
proved ver\- valuable for studying problems of relapse and treatment
of malaria in man.

The time required for the completion of the sexual cycle in the
mosquito varies \Nith the temperature. Under certain conditions it may
take only five days for a female mosquito to become infective, but in
other cases sporozoites only appear in the sahva after two months have
elapsed.

Some species of bird Plasmodium, of which P. relictum is a good
example, are easily transmitted to different kinds of birds, but others
show more or less ^^-ell-marked host specificity'. P. gallinareum, which is
a parasite of the fowl, will not develop naturally in any other bird,

PROTOZOA 169

although geese have been infected by inoculating them with the blood
of an infected chicken. The cliff-swallow [Petrochelidon albifrons) from
America is a bird with a strictly host-specific Plasmodium^ which, up to
date, has not been recorded from any other bird.

These various species of bird Plasmodium, and in fact most of the
parasitic forms, can only be studied and identified after submitting
them to elaborate staining processes. Without the sharp contrasts
produced by artificial dyes the minute structural differences would
remain invisible to the human eye. A drop of blood from an infected
bird is spread thinly on a glass slide and then dried. Subsequently this
film is treated with certain dyes to which the various parts of the blood
cells and the parasite react in a particular manner.

The different species of bird Plasmodium are separated on such
characters as the shape of the gametocyte, the number of merozoites in
one cell, the shape of the pigment granules and other similar types of
peculiarities. It is a matter of considerable difficulty and the accurate
identification of Plasmodium is unquestionably a matter for a highly
trained specialist.

The allied genera of bird malaria parasites. We have already mentioned
that the unfortunate class Aves is afflicted by two allied genera of
Protozoa, to which man is luckily immune. One of these, Leucocytozoon
(Fig. 2,b), was found by Coles to be the commonest parasite in the blood
of British birds. It is recorded from a number of hosts including the
thrush, blackbird, jay, starfing, blue-tit, moorhen, pigeon, grouse,
tawny owl and brambling. Swallows are especially susceptible and
possibly acquire their heaviest infections if they gather in flocks in reed
beds prior to autumn migration — for, as nestlings, they are free of
infection. About 68 species of Leucocytozoon have been named, all of
which are confined to birds. In the United States it is sometimes the
cause of fatal epidemics among domestic ducks and turkeys. The
known insect-vectors are species of black-fly [Simuliidae) .

The genus Haemoproteus (Fig. 2,c), which also parasitises reptiles, has
been found in the blood of various wild birds in Britain including the
chaffinch, thrush, blackbird, starling, wood-pigeon and grouse. About
45 species have been described and named from various countries, but
many of these are probably only new names for "old" species. Haemo-
proteus is widely distributed and very common — a fact which is readily
appreciated when it is realised that in the United States this parasite is
found in 50 to 60 per cent, of certain thrushes and in 80 per cent, of

lyO FLEAS, FLUKES AND CUCKOOS

mourning-doves {^enaidura carolinensis) . Over 500 different species of
birds have been recorded as hosts. The only known insect carriers, in
which the sexual cycle occurs, are louse-flies (Hippoboscidae).

In Haemoproteus the adult gametocyte encircles the nucleus of the
red blood corpuscles like a halter. This characteristic stage induced an
early worker to bestow the name Halteridium upon the parasite — a name
by which the group is still often known. In the case of this genus and
Leucocytozoon the only forms of the parasite which are found in the red
blood cells are the gametocytes. For this reason these two genera, un-
like the malarial parasites, cannot be transmitted in the laboratory
from bird to bird by injection of blood. Transmission occurs only as a
result of a bite by an infected insect carrier. The stages of the asexual
cycle (schizogony) are passed in the endothelial tissues. Some author-
ities have consequently divided off the two genera Leucocytozoon and
Haemoproteus from Plasmodium and placed them in a separate family,
Haemoproteidae.

Other Sporozoa

Another group of Sporozoa, Toxoplasma, which infects the white
blood corpuscles and various tissues, has been recorded from many wild
birds, including the English sparrow in the United States. It has been
found in two captive squirrels in this country but has not been studied
in birds. Haemogregarines and Piroplasms, which are also parasites in
the blood of avian hosts, may eventually be found in British wild
birds. Both groups have been recorded from wild mammals in this
country.

Glass Mastigophora (Flagellata)

The Protozoa which are included in this class are known as flagel-
lates, for, typically, they possess one or more flagella. Each flagellum
consists of a fine whip-like outgrowth which is capable of lashing or
rippling movements, by means of which the organism is enabled to
progress through the liquid medium in which it lives. Sometimes
flagella are used as organs of attachment rather than locomotion.

The majority of Mastigophora have a single nucleus. They are
chiefly free-swimming and many of them live in the body fluids of

PROTOZOA 171

Other animals. Reproduction is usually by binary fission, the animal
dividing into two by splitting along the longitudinal axis.

In the case of parasitic forms the life-cycle may involve development
in an intermediate host.

Order Protomonadida

As far as birds are concerned the most important flagellate parasites
are concentrated in this order. Of these the best known belong to the
family Trypanosomidae (Plate XXV), which are parasitic in verte-
brates, invertebrates and certain plants with a milky "juice" in their
stem and leaves. The only genus recorded from British birds is
Trypanosoma (see tail-piece of Chapter 9). Under the microscope
these parasites superficially resemble little fish — with a long, un-
dulating crest in place of a dorsal fin. The fi.agellum runs along the
outer margin of this membrane and projects beyond it as a free lash. On
a slide some species can be observed wriggling sluggishly among the
blood corpuscles while others dart about like lively minnows. Try-
panosomes have no mouth (cytostome) and their food is absorbed in
liquid form through the cell membrane. The life history of the species
from birds has not been fully worked out. Like the majority of try-
panosomes, they occur chiefly in the blood, but in some cases they have
also been found in the bone marrow and other tissues of the vertebrate
host. Generally the birds appear to be unharmed by their presence but
in the laboratory when unusual hosts are used death may follow an
artificially produced infection

The genus Trypanosoma is very common in birds and has been
recorded from over 200 species. It is customary to name each one of
these as if it represented a host-specific trypanosome. Thus, for example,
the one found in the chaffinch is named T.fringillinarum. In all proba-
bility the same species occurs in a number of diflferent hosts as the
organisms in question are very variable (polymorphic). In Britain
Trypanosoma has been found in the rook, jackdaw, yellow-hammer,
chaffinch, linnet, blackbird, jay, thrush, house-martin and swallow.
In Germany it has been recorded from many other birds on the British
list, and is often present in the blood of nestlings only a few days old.

Most trypanosomes are transmitted by invertebrate hosts. For
instance, a trypanosome of sheep is carried by the sheep ked (a louse-
fly), one from the rat by fleas, one from the tortoise by leeches, another
from the camel by horse flies and the most famous of all trypanosomes.

j-72 FLEAS, FLUKES AND CUCKOOS

those which produce sleeping sickness in man, and nagana in cattle, are
transmitted by tsetse flies. Only one of the horse trypanosomes, T.
equiperdum, is known to have a direct life-cycle and passes from horse
to horse during the sexual act. In the invertebrate host these parasites
develop in the alimentary canal, finally giving rise to the infective
forms. In some trypanosomes the latter are produced in the mouth
parts or salivary glands, and are then inoculated into the vertebrate
during the blood meal. In others, well illustrated in the rat flea
infected with T. lewisi, the infective forms develop in the hind gut, and
infection occurs when the host accidentally ingests the flea or its drop-
pings. It is beheved that trypanosomes have evolved from a more
primitive type of flagellate which is normally parasitic in the gut of
insects. During the part of the cycle within the invertebrate host the
trypanosomes pass through various stages in which they appear to
revert to ancestral forms.

The carriers of bird trypanosomes are not known for certain. Some
development appears to take place in mosquitoes and it has been
claimed that T. loxiae and T. noctuae (from the crossbill and little owl)
multiplied and produced crithidia-like forms after ingestion by the
house-gnat. It has been claimed that the red mite {Dermanyssus gallinae)
can transmit one species of bird trypanosome. The fact that nesdings are
so frequendy infected in nature suggests that the carrier is an arthropod
breeding in their nests.

Very often the blood of wild birds is infected with various sorts of
parasites. One thrush examined by Coles was found to harbour
simultaneously all three genera of bird malaria parasites {Plasmodium,
Haemoproteus and Leucocytozoon) a Trypanosoma and a filariid worm. This
is confusing, and even trained scientists have fallen headlong into the
trap and have described, with great enthusiasm, completely different
organisms as stages in the life-cycle of the same species.

Another well known parasite from the same order is Histomonas
meleagridis.This is a flagellate with an amoeboid phase, harmless if present
in the intesdne of chickens; but in turkeys it invades the liver and
intestinal wall, causing a mortal illness commonly known as "black-
head." It does not form a cyst but is transmitted directly when a bird
accidentally ingests contaminated faeces or the eggs of the caecal
worm [Heterakis) which act as transport hosts.

There are also numbers of Trichomonadidae (Fig. 2,d) found in
birds. These are spindle- or pear-shaped flagellates with a sdff rod-like

PROTOZOA 173

axostyle supporting the body^ several free anterior flagella and an
undulating membrane bordered by a marginal flagellum. They divide by
simple fission and no sexual phenomena have been observed. They do
not form cysts but remain alive long enough outside the body to effect
successful transference to new hosts. In the intestine of various birds,
species like Trichomonas gallinarum ingest debris, bacteria and other solid
particles and are apparently harmless, although on rare occasions they
invade the liver with disastrous consequences. A species, T. gallinae,
from the mouth, throat and oesophagus of birds such as gulls, falcons,
pigeons and poultry, appears to consume leucocytes and attacks the
mucous membrane, and T. columbae, from the crops of pigeons, is
closely related to a species found in the vagina of Homo sapiens.
Another related species, T. foetus, infecting the uterus and penis of
cattle, is an important cause of abortion in cows.

Other flagellates found in the intestine of birds include forms such
as Chilomastix gallinarum (Fig. 2,e) from the caecum of the fowl and
Cochlosoma anatinis from the intestine of mallard, shoveller, pintail, scaup
and other duck.

Order Diplomonadida

The flagellates from this order are strikingly different from all the
others. Owing to a duplication of certain organs they are bilaterally
symmetrical. This gives the impression that the animal is in the process
of longitudinal fission.

Giardia (Fig. 2), which is the best known genus, superficially re-
sembles a pear split in half, with eight flagella arranged in pairs arising
from different parts of the body. It clings to the epithelial cells lining
the small intestine by means of a sucking disc. Apparently it stimu-
lates a copious secretion of mucus upon which it subsequently feeds.
Intermittently it forms cysts which pass out in the faeces and are thus
transported to other hosts. Giardia is found in vertebrate animals
throughout the world and has been recorded from a variety of bird
hosts including the common buzzard, shrike, avocet and several species
of herons. The allied genus Hexamita has also been recorded from birds.

Class Rhizopoda
This class comprises some of the simplest Protozoa known as amoe-
bae. The body has no definite shape or orientation, but assumes a

1-74 FLEAS, FLUKES AND CUCKOOS

globular form when at rest. Amoebae move and eat their food by
means of pseudopodia. Part of the cytoplasm is pushed outwards until
it protrudes like a finger. Then the rest of the body flows into it and
thus the organism can move slowly from one place to another. By
means of these pseudopodia they also encircle particles of food such as
bacteria, cysts of other Protozoa or blood corpuscles and subsequently
ingest them. Owing to the fact that these naked blobs of protoplasm are
the first living animal the average naturalist examines under the micro-
scope, they are, to most of us, objects of great affection and nostalgic
pleasure.

Although most amoebae are free-living in soil and water, the
majority of vertebrate animals harbour either commensal or parasitic
forms in their large intestine. In man there is one highly pathological
species which lives on red blood corpuscles and is the cause of so-called
amoebic dysentery. The only family which includes important bird
parasites is the Amoebidae (Fig. 2,i). The best known British species
from \vild birds is Entamoeba lagopodis from the intestine of the grouse.
iMultiplication occurs by binary fission. The organism elongates and
then splits in two. Cysts with four nuclei are formed and these pass
out of the grouse with the faeces. They contaminate drinking water and
food and are thus ingested by new hosts. The amoebae themselves can-
not survive outside the body.

Various other species have been described, from fowl, domestic
ducks and geese, and certain wild birds, with cysts showing one, four
or eight nuclei.

The foregoing account of the Protozoa from birds scarcely does the
group justice. A great deal has to be compressed into a small space, the
terminology is necessarily technical and the subject matter so compli-
cated that little more than a straightforward factual account can be
given. Undeniably the chapter makes dull reading. To dispel this im-
pression Protozoa have only to be looked at alive under the microscope.
Most people instantly fall under their spell. The great majority of these
organisms are colourless and in studying them one enters a fascinating
world of relative transparencies. Every species displays some subtle
difference in opaqueness, density, refraction or translucence. Protozoa
move in countless different ways. Some dash across the field of vision
like express trains, some corkscrew around in never-ending spirals,
some flicker intermittently like summer lightning, others swim by the
rhythmical beating of countless transparent ciha, or lash their way

PROTOZOA ly^

about in jerky spasms ; many move by sinuous and beautiful undulations.
Others again push out portions of their own bodies and let their proto-
plasm stream into the protuberance — thus slowly flowing from place to
place. In order to get some idea of this beautiful, obscure and animated
crowd it is only necessary to smear a little of the mucus from the crop,
intestine, cloaca or other body fluid of a bird on to a wet slide and focus
the microscope.

Trypanosoma gallinarum from the fowl
(after Wenyon) (x 2000)

CHAPTER 10

WORMS (VERMES)

In all these the nobler organs seem of such little use, that if
they be taken away the animal does not appear to feel the
want of them.

Buffon's Natural History

WORM has become a term of abuse. In the modern world it conjures
up a picture of a henpecked husband or the fellow who lives
to fight another day, or something pale and elongated, wriggling in
distress when a stone or a piece of decaying meat is turned upside down
in the sunshine.

From the naturalist's point of view the term is applied somewhat
loosely to four phyla of animals : Platyhelminthes or flatworms, among
which are found the tapeworms and flukes ; the Nemathelminthes or
roundworms, which include the nematodes ; the Acanthocephala or
spiny-headed worms, and Annelida or segmented worms, which include
earthworms and leeches.

The tapeworms, flukes and spiny-headed worms are exclusively
parasitic, although some of their larvae enjoy a few hours of careless
freedom in the water and their eggs are washed about the world in the
ebb and flow of urine and faeces.

During the course of their evolution most of the parasitic worms have
been forced to become efficient egg machines, but this has not by itself
solved the problem of their survival. Despite the vast number of ova
they produce, both tapeworms and flukes have had to resort to other
methods by which their progeny can be further multiplied. Thus, by a
process of asexual reproduction (fragmentation of the germ cell) inside
the first host, one egg of a bird trematode can give rise to several
million free-swimming larvae, each capable of developing into a
complete adult. Some tapeworms bud off^ multiple individuals in the

176

WORMS 177

larval stage as well as adding new segments in the "neck" region —
which is also a form of asexual multiplication.

During their complicated history as parasites all the digenetic
flukes, tapeworms and the spiny-headed worms have become involved
with various intermediate hosts. In some cases it is difficult to say
where the process first began. Possibly the bird, which is now the final
host, was a later addition to the original life-cycle and tagged on at the
end. It is obvious that by persistently eating an animal infected with
flukes a bird must again and again expose itself to infection. Despite this
fact, it is sometimes difficult to imagine how the change from inverte-
brate to vertebrate host can have occurred, but an important clue has
been provided by experiments carried out by Baer. He has shown that if
the tapeworm Ligula intestinalis (see p. 195) is "cultured" in an artificial
medium, and the temperature raised, the larval form will lay eggs
precociously (progenesis) . In view of these experiments it is relatively
easy to visualise how, when the worm was introduced into a vertebrate,
the sudden change of environment could stimulate egg-production and
enhance the species' chances of survival. Under such circumstances the
vertebrate host could enter the life-cycle permanently and supplant the
original "final" host. There is another advantage which vertebrates
enjoy over many invertebrates : on the whole their life is longer, and
each individual thus provides the internal parasite with protection and
food over a more extensive period. Vertebrates often wander far
afield; consequently the parasites which keep up continuous egg-
production are enabled to scatter their eggs over a much larger area and
during a longer period, if they are lodged, say, in the intestines of a bird
instead of the body-cavity of a fly. If man fed regularly upon insects
he would probably have acquired many worm parasites which are
at present found chiefly in insectivorous birds, but also in bats and
other animals, with similar tastes. Hands have relieved him of the
grim necessity of eating his own ecto-parasites — otherwise he might
easily have become infested with the rat and dog tapeworms which
use fleas as intermediate hosts.

In discussions on parasitism it is customary to compare an ill-
adapted parasite, which kills the host, with the farmer who killed the
goose which laid the golden eggs. In the case of flukes and tapeworms
it is equally important from the point of view of their race that the
host should survive in order that they can continue to lay their "golden"
eggs, for the bird — by scattering them far and wide in urine, faeces and

1^8 FLEAS, FLUKES AND CUCKOOS

exudates — counteracts or at any rate minimises the effects of the para-
site's isolated and stationary existence.

In many cases it seems probable that intermediate hosts have been
secondarily interpolated in the life-cycles merely because they provide
the most accessible route to the final vertebrate host. It is a striking
fact that almost all complicated life histories involve endo-parasites.
Ecto-parasites, whether they are flukes on the gills offish, or feather lice
on the quills of birds, generally have a direct and simple life-cycle. It is
likely that endo-parasitism, whether the habit arises suddenly or
gradually (see p. 48), always tends to involve intermediate hosts. It is
often the easiest way, maybe in some cases the only way, of getting in or
out of the host's body successfully. A filariid worm not only has to
deal wath the difficulty of finding a final host which is relatively isolated
in space, but has to contend with the greater isolation imposed by con-
finement within the tissues and bloodstream of the host. The insect
vector is one of the few possible solutions. By whatever curious paths
the present situation evolved, it is now sufficiently complicated and
extraordinary to satisfy the imagination of Salvador Dah himself In
order to complete their life-cycles many flatworms must pass through
three different hosts, which may even include one living in the water,
another on land and a third flying in the air. Moreover, many of the
flukes which, in some stages, may be no bigger than a grain of sand, can
only survive in extremely circumscribed areas of the host's body, such
as the tentacles of a snail, or the eye of a fish, or the bile duct of a bird.
When the flatworms gave up their freedom they certainly began an
odyssey compared with which the voyages of Ulysses seem singularly
uneventful and commonplace.

Nematodes are the most important group of worms parasitising land
birds generally, and exceed in variety and numbers all the others put
together. They are found in a large assortment of vertebrates and
arthropods, ranging from camels to bumble-bees, and are in no way
confined to birds. In this book no attempt is made either to list the
species of parasitic worms found in British wild birds or to give an
account of their morphology and classification. Thousands of species
are involved and all that space permits is to focus attention on a few
nteresting points concerning each of the major groups.

J . G. Bradbury

a. Fluke, Cryptocotyle lingua, from
intestine of herring-gull ( x 49)

S. C. Porter

b. Roundworm, Syngamus trachea, male and
female in copula ( x 2-5)

S. C. Porter
c. Tapeworm, Dilepis undula, from intestine of song-thrush ( x 2-9)

PlaU XXVII

WORMS

D. P. Wilson

a. Common periwinkle, Littorina liltorea ( x 0-37)

D. P. Wilson

b. Common goby, Gobius jninutus ( x i -G^)
INTERMEDIATE HOSTS OF THE HERRIXG-GULL FLUKE, Cryptocotyle lingua
Plate XXVI 1 1

WORMS 179

Roundworms (Nematoda)

The roundwoi-ms, as we have ahxady noted, are placed in a separate
phylum Nemathelminthes. Although in the popular sense they are
quite obviously "worms" a man has more in common with a snake than
a roundworm has with a flatworm. Large numbers of nematodes are
free-living and are to be found teeming in the soil and water. Their
morphology is generalised and rather unspecialised — a fact which has
puzzled a great many biologists. Some have concluded that all free-
living nematodes are derived from parasitic forms, while others see in
the relative simplicity of their anatomy a pre-adaptation to the parasitic
mode of life. A great deal of confusion exists, however, in the minds of
various writers on the definition of adaptation and modification, as the
two following quotations, taken from the works of two leading authori-
ties and both published in 1946, will show. One writes : " The majority
of the parasitic forms are relatively giants and are often much modified
by their parasitic life." The other writes : " The nematodes, on
account of their simplified anatomy, appear to have escaped the effects
of parasitism."

Roundworms are cylindrical, generally tapering to a point at both
ends. They have a well-developed intestine, a body cavity and— with
few exceptions— the sexes are separate. The females are generally
larger than the males and the latter have differently formed tails, often
with a saucy curl at the tip. Occasionally, there is a marked sexual
dimorphism. The females of the blood red spirurid Tetrameres found in
the proventriculus of many wild birds are almost globular, whereas the
males retain the typical cylindrical shape. One male nematode
{Trichosomoides) which is parasitic in the urinary bladder of rats lives
a life of ease inside the vagina or uterus of its own female. The cuticle,
although transparent, is tough and apparently impermeable— in many
cases reminiscent of the cuticle of arthropods, although it is not
chitinous. This cuticle is sometimes expanded into fin-shaped flaps,
which are useful for purposes of classification.

The life-cycle of the nematode is simple compared with that of the
fluke or tapeworm. Although, between the egg and the adult worm,
there are four moults and the successive larval stages may diff'er in
minor structural details, there is no alteration of distinctive larval
generations or asexual multiplications either by budding or poly-
embryony. Their tgg production is, however, higher than many of the

FFC— N

l80 FLEAS, FLUKES AND CUCKOOS

flukes and tapeworms and it has been estimated that a large individual
nematode from man can lay over 27,000,000 eggs. Sometimes develop-
ment is direct, but unlike the free-living nematodes, the parasitic forms
often require intermediate hosts in order to complete their life-cycle.
There is another extraordinary phenomenon well known among nema-
todes, of which the Ascaris from man, affords the best known example.
When an Q;gg of this worm is swallowed by the host it hatches in the
small intestine, the site where eventually Ascaris spends its adult life.
However, it appears incapable of developing to maturity without first
undertaking a ten-day peregrination inside the host's body. After
penetrating the mucous membrane of the intestine it is caught in the
bloodstream and swept into the liver, thence to the heart and lungs.
Possibly in this location it finds additional oxygen which is necessary
for its development — but this is a matter of pure conjecture. The
young Ascaris then burrows out of the lungs into the trachea and event-
ually regains the intestine via the throat and oesophagus, where it
continues development. Similar apparently meaningless migrations
inside the host's body are undertaken by many nematodes. Some
authors put forward the view that this is an extension of a "burrowing"
habit exhibited by most of these worms at some period of their develop-
ment. They may burrow into the mucosa lining the intestine and then
return to the lumen or merely bury their heads in it, or burrow directly
through into the body cavity, or burrow into the tissues of an inter-
mediate host. Other authors believe that the extensive migrations can
be explained on the assumption that these nematodes originally became
vertebrate parasites by burrowing through the skin, or that at some
period of their history the species in question developed in an inter-
mediate host. Now the cycle has been curtailed but the larva still takes
a trip which has become redundant since the intermediate host has
dropped out. One thing appears certain — these migrations through the
host are no joy rides. Like the charge of the gallant Light Brigade —
hundreds set out on their apparently pointless mission but only a few
come back.

Chickens are excellent hosts for roundworms and over 50 species
have been recorded from the fowl. A rapid glance at any manual
deahng with the diseases of poultry gives a good idea of what we can
expect in wild birds with the same sort of feeding habits.

Perhaps the best known of all bird nematodes is Syngamus trachea
(order Rhabditida, sub-order Strongylina), a brilliant scarlet worm

WORMS l8l

about the length of a pin which Uves fixed in the trachea of the host and
is the cause of the disease known as the gapes. Chickens can become
infected in two ways. Either they ingest embryonated eggs which have
passed out with the bird's droppings and have developed while lying on
moist ground; or they can eat earthworms into which the recently
hatched larva has penetrated and subsequently encysted. Various
authors claim that birds are easier to infect in the laboratory if they are
fed with earthworms containing cysts, rather than the embryonated
eggs. House flies, green-botde flies, springtails and centipedes also act
as transport hosts. When infected they become sluggish and are easily
caught. Certainly in nature birds can become infected by both the
direct and indirect method. After the gapeworm has been swallowed
by the avian host it escapes from the intestine and migrates — possibly
via the blood stream — to the lungs. Some time is spent in this site before
the worm moves on and takes up its final position in the windpipe.
Sygnamus copulates while still immature and the male and female remain
joined together for hfe, thus forming a characteristic Y-shaped figure
(Plate XXVIIb). Only a portion of ingested embryonated eggs reaches
maturity. From 10,000 larvae fed to a turkey only 235 pairs were
recovered from the windpipe and lungs — but this was sufficient to kill
the host. The gapeworm is a cosmopolitan species of which there may be a
number of different wild strains. The most highly infected hosts in
Britain are rooks and starlings but there have also been records from
the robin, little owl, magpie, jay, carrion-crow, jackdaw, kestrel, house-
sparrow, purple sandpiper and several others. Young birds are much
more susceptible than adults and often a very high proportion of nest-
lings harbour these worms, whereas only a small percentage of the
parent birds in the same population are infected. In the case of
partridges the females are more susceptible than males. An allied
species, Syngamus merulae, is found in thrushes and blackbirds in
Britain.

Another well known parasite of the chicken and wild birds, which is
also placed in the same order, is Trichostrongylus pergracilis. This is a
small species less than a centimetre in length which may be found in
thousands in the caeca of infected birds. In Britain it has only been
recorded from the grouse and occasionally the partridge. The life-
cycle is direct. The eggs pass out with the droppings and hatch in about
two days. Two moults take place and at the end of a fortnight the
larvae become infective. When the dew is on the grass or after rain they

r82 FLEAS, FLUKES AND CUCKOOS

wriggle up the stems of heather or some other suitable plant and wait.
A grouse, partaking of an early breakfast, inadvertently swallows the
larvae which on reaching the caeca undergo two further moults and
become adult worms.

One of" the most interesting worms found in the caeca of chickens
and also in wild birds such as the coot is Strongyloides avium. In this whole
family there is a most peculiar life-cycle which may possibly throw a
little light on the evolution of parasitic nematodes.

The eggs hatch after being voided with the faeces and young worms
develop in the soil into both adult male and female free-living
individuals. These worms copulate and lay eggs which in turn give rise
to larvae which feed, moult and develop into another generation of free-
living worms. This process may be repeated several times but sooner or
later a different type of larva is produced, which, if ingested by the right
host, develops into an outsize parasitic female which reaches maturity
inside the bird and lays parthenogenetic eggs. No parasitic male has
ever been found.

The worms of this family seem to form a link between the free-living
and parasitic forms of nematodes. It is uncertain what causes the
production of the parasitic types of larvae, but experiments on allied
species suggest that abundance of food and certain other environmental
factors influence the course of development. Some strains of the same
worms seem more susceptible to a luxurious environment than others
and abandon the free-living life and produce parasitic forms more
readily. Caullery has suggested that all the special types of reproduction
so characteristic of parasites, such as parthenogenesis, polyembryony,
strobilisation, budding and so forth, occurred originally because of the
particular type of environment in which the eggs happened to develop
— conditions not necessarily linked with parasitism, but characters
which subsequently made adaptation to such a precarious life possible.
Many of the Strong)data are bright red in colour — due to their habit
of sucking blood from their hosts. They bite the intestinal wall or seize
it in their mouths, simultaneously pouring out a secretion which
prevents coagulation of the blood. They may also perhaps obtain a
supply of oxygen, which is lacking in the intestinal tract, by keeping up
a constant flow of blood through their bodies. Some species have the
power of digesting the tissues of the host without first swallowing them.
The secretions of their oesophageal glands are poured out and they then
imbibe the pulpy, semi-liquid mass produced in this manner.

WORMS 183

The superfamily Ascaroidea is also well represented both in chickens
and wild birds. The best known of all the worms of poultry is the caecal
worm Heterakis gallinae, notorious as the carrier of Blackhead disease
[Histomonas meleagridis) . This worm has a direct life-cycle and the
eggs, after a period of incubation on the ground, will hatch in the
intestine of susceptible birds if they are swallowed in food or water.
Within twenty-four hours the larva has reached the caeca and
penetrated the mucosa, where it remains for two to five days. It then
returns to the lumen of the caeca where it spends the rest of its adult life.
Various related species are recorded from British wild birds such as the
sheld-duck, tawny owl, curlew, various geese and game birds. Earth-
worms frequently ingest the eggs and may act as transport hosts.

Heterakis is a relatively small worm, only a few millimetres in length.
Worms of the genus Ascaridia are, however, much longer, sometimes
four to five inches long. A. galli is one of the commonest worms in
poultry and there are many related species in wild birds, especially in
game birds such as the capercaillie [Tetrao urogallus) but also in some
passerines. Young birds are much more frequently attacked than older
ones and it has been shown that after goblet cells are developed in the
epithelial lining of the duodenum the birds seem to become relatively
resistant to infection. Diet also has a considerable influence on the rate
of infection and when deprived of vitamins or animal protein the birds
easily become parasitised by these worms.

The food of the Ascaroidea, unlike the Strongylata, consists
principally of the intestinal contents rather than the blood or the mucous
membrane of the host. Several experiments have been planned to
prove this. Infected chickens have been fed on beef and charcoal and
both ingredients were subsequently recorded from the intestines of the
nematodes. On another occasion a certain number of chickens infected
with A. galli were fed by injections and only given water by mouth. In
these birds the worms failed to grow, while in the control chickens,
which were fed in the usual manner by mouth, the parasites grew
normally.

There are, of course, numbers of related roundworms (Ascaroidea)
which are not found in poultry. The genus Contracaecum is characteristic
of fish-eating mammals, birds and predatory fish. C. spiculigerum is a
cosmopolitan species found in the proventriculus of cormorants and
other sea birds such as auks, guillemots and skuas. Fish serve as first and
second intermediate host. Another closely related genus, Porrocaecum,

184 FLEAS, FLUKES AND CUCKOOS

which is also recorded from seals and fish, parasitises a wide variety of
birds in Britain. P. depressum uses moles and shrews as second inter-
mediate host and birds of prey, such as the peregrine falcon and tawny
owl, as the final host.

Chickens harbour a nematode in their eye, another in their crop,
stomach, gizzard and intestine, which belong to the order Spirurida —
an order which contains only parasitic forms. All these worms require
an intermediate host in order to complete their life-cycle. Oxyspirura
mansoni, which has been chiefly recorded from game birds and domestic
poultry, lays its eggs in the eye of the bird and they are subsequently
washed down the tear ducts and swallowed, eventually passing out of
the bird's body with its droppings. Cockroaches — and possibly other
insects — which are notoriously "dirty" feeders, ingest the eggs. About
two months later mature larvae are present in the insect. Sometimes
they are encysted in the fatty tissues and along the alimentary canal and
at other times free in the legs or body cavity. When the cockroach is
eaten by a susceptible bird the larvae are freed in the crop. From there
they migrate up the oesophagus and through the tear duct leading from
the nose to the bird's eye. Larvae may reach the eye only twenty
minutes after the infected cockroach has been swallowed. A related
species, 0. sygmoidea, is found in crows and rooks.

The blood red proventriculus worms ( Tetrameres) live in the glands
of the stomach. The females are globular and fit snugly inside the glands,
but the males, which are almost microscopical in size, have the
typical nematode shape. They often remain attached to the surface of
the stomach wall and only penetrate inside the glands for the purpose of
copulation. One species, Tetrameres fissipinus, is found in various wild
birds in Britain, chiefly in goosander, pochard, coot, grebes and other
aquatic feeders. In this case a number of different intermediate hosts
are used. Those favoured are the water fleas {Daphnia pulex), and
fresh water shrimps {Gammarus pulex) , but earthworms, grasshoppers and
various other insects are used by the species parasitising poultry.

Another common parasite found in the proventriculus of wild birds,
especially raptorials, is Acuaria laticeps. It is reported from the kestrel,
peregrine falcon, short-eared owl and barn-owl in Britain. Other
species of the same genus are found in swallows and martins, another
from wood-peckers, herons, and crows (including nutcrackers), and
shrikes. The various species are often characteristic of one family of
birds. The wood-louse [Armadillium vulgare) is the intermediate host for

WORMS 185

A. Spiralis, but various invertebrates such as Gammarus pulex may be
used as host. In the case of the well known gizzard worm, Acuaria
hamulosa, which is generally located near the opening between the
stomach and intestine, chickens become infested by eating various
insects, like weevils and grasshoppers.

The blood of many wild birds is found to be teeming with larval
Spiruroids known as microfilariae. In Britain these larvae have been
recorded from blackbirds and thrushes and the rate of infection was
said by Coles to be very high. In the United States 60 per cent, of a
population of wild crows was found to be infected with microfilariae
The adult worms live in the connective tissues or body cavities of the
host. The female gives birth to free-living embryos, the microfilariae,
which swarm in the blood where they await ingestion by a blood-
sucking insect, which, in the case of the species infecting man, is a
mosquito. Inside the intermediate host they undergo further develop-
ment and, after a certain period, assemble in the proboscis of the mos-
quito. During the insect's next blood meal they break loose from the
mouth-parts and creep out on to the skin of the host. They quickly
penetrate through the mosquito " bite " or any other abrasion and by an
unknown route return to the original site of infection. In certain of the
species infecting man there is a diurnal periodicity in the appearance of
the microfilariae in the peripheral blood stream. During the day
scarcely any are present, but at night between 10 p.m. and 4 a.m. they
teem near the surface of the body. Nobody has so far discovered what
mysterious influence drives them outwards, but as certain species of
mosquito only bite at night, it has been suggested that this is an adjust-
ment of the life-cycle which brings the larvae into contact with these
insects. There, while their host sleeps, they wait like expectant
lovers.

Some ingenious person has, with the aid of a microscope, watched
microfilariae in the transparent web of a frog's foot. It was seen that
they work up the capillaries against the blood stream and are apparently
actively attracted to the saliva of the insect vector, which it pumps into
the wound at the moment of biting. In the case of Onchocerca — a mam-
malian Spiruroid carried by blackfly — the microfilariae swarm im-
mediately below the epidermis.

The life-cycles of the numerous species from birds are not known,
but as those from man, frogs and lizards are carried by species of gnats
{Culex) it is highly probable that they follow a similar course in avian

l86 FLEAS, FLUKES AND CUCKOOS

hosts. It is also not known whether the microfilariae in birds swarm
periodically as they do in man.

The members of the order Enoplida are often called whipworms
because, in some species, the posterior end of the body is thickened and
looks superficially like the handle of a whip, while the narrow slender
anterior portion is reminiscent of the thong. They are found in a wide
range of hosts and in some queer situations. The best known whip-
worm is Trichinella spiralis, which is the cause of a serious, sometimes
fatal disease in man, and which is contracted by eating underdone,
infected or so-called "measly" pork. When the-Hfe cycle of this worm
was discovered in 1828 it was thought that a great light had been shed
on the ancient Hebrew law which bans the consumption of pig. This
superficial and facile explanation is made without any foundation,
although some scientific books declare it is "without doubt" true.

Trichurata are particularly common in the crops and intestines of
birds. The most familiar genus is Capillaria, and needless to say, the
unfortunate chicken has its full share of this particular trouble. These
worms live more or less embedded in the intestinal mucosa. One of the
best known species is C. columbae, a hair-like worm less than half an inch
in length, which also infects pigeons and peacocks. The life-cycle is
direct. The eggs require several days to become infective but only hatch
after being swallowed by the host. They enter the mucosa of the duode-
num and complete development there before returning to the lumen of
the intestine. In certain species, such as C. annulata, infecting the
crops of chickens and other birds, the embryos have to mature in-
side earthworms which serve as true intermediate hosts. There are
also various species of Capillaria which undertake long migrations
through the host's body before taking up their final position. A com-
mon species in British wild birds, ranging from buzzards to robins, is
C. contorta. The genus is one of the largest and infects mammals as
well as avian hosts.

Chickens with heavy infections of Capillaria show an inclination for
solitude, become extremely thin, and eventually die. Although many
species of worm appear to have little or no effect on their bird host, this
is, in all probabihty, because we cannot ask them about their symp-
toms. Heartburn, dizziness, insomnia, optical illusions, general
nervousness, flatulence, abdominal discomfort, reduced perspiration,
palpitations of the heart, dirt-eating and loss of vitality due to nematode
infections are listed in a book on human parasitology. This type of

WORMS

187

symptom is scarcely likely to be recorded for birds harbouring similar
parasites. Mechanical injuries, such as perforation of the intestinal
wall, severe bleeding, irritation and inflammation of various tissues,
blocking of ducts, thickening or maceration of various internal sur-
faces, the formation of ulcers or even cancerous growths are the types of
injury which attract attention. In nature, however, birds, unlike the
barnyard fowl, are not generally subjected to conditions which favour
infection with large numbers of nematodes simultaneously. It must also
be remembered that infections only last for a limited time, generally
less than a year. In due course the worms die and except in a few cases
they do not multiply inside the host. Therefore, if only one or two
specimens are present at one time, the bird probably recovers from the
injuries they inflict and symptoms due to their toxic secretions cease
when the parasites are eliminated. Nevertheless, when a bird-watcher
puts up his glasses to watch starlings or rooks feeding in the fields he
should pause and feel grateful that, unlike the birds, he can cook his
breakfast.

Shore crab, Carcinus maenas,
the intermediate host of several worms infecting birds (x .5

l88 FLEAS, FLUKES AND CUCKOOS

Spiny-Headed Worms (Acanthocephala)

The spiny-headed worms which are of rather uncertain affinities —
sometimes placed with the roundworms, sometimes with the flatworms —
are also well known internal parasites of birds. They are round,
smooth, unsegmented worms, with a large retractable proboscis, armed
with closely set, ferocious looking hooked spines, which they force into
the lining of the host's intestine and which acts as a powerful organ of
attachment. Unlike other flatworms, they have a body cavity and the
sexes are separate, but they share with the tapeworms the total absence
of an alimentary canal at all stages of development. The females
produce large numbers of eggs which lie free inside the body. Situated
at the posterior end of the worm is a complicated organ which sorts out
the eggs like a superior type of potato riddle — the embryonated ova are
passed to the outside and those which are undeveloped are returned
again and again to the inside of the worm's body until they have fully
matured.

Unfortunately very little has been discovered about their physi-
ology but they are known to carry more fatty substances in their tissues
than any other group of helminths. It is hoped that in future parasitol-
ogists will give more attention to the physiology of endoparasites in
general, for in the process they are bound to make fundamental dis-
coveries concerning not only the parasites themselves but the bio-
chemistry of the alimentary canal and other organs of the host.

Compared with the other parasitic helminths the spiny-headed
worms form a small group totalling less than 250 species in all. The
popular writer sighs with relief when he considers the nine acanthoce-
phalids (all from the family Polymorphidae) recorded up to date from
birds in Britain. A further thirty odd species (four families) from North
and Central Europe have been found in birds on the British list. In all
probability these will turn up in this country during the course of
collecting.

The spiny-headed worms are chiefly parasites of aquatic vertebrates.
The vast majority employ Crustacea as the first intermediate host, and
are found as adults in the intestines of fish, amphibians, seals, whales
and water birds. A fair number, however, have become adapted to
terrestrial animals and they then use insects as intermediate hosts.
Among the nine species from British birds six are from aquatic or semi-
aquatic hosts, one from birds of prey, and two from passerines. A typical

WORMS 189

example is Polymorphus boschadis recorded in this country from the
sheld-duck, mute swan, gadwall, scaup, garganey and domestic duck.
The eggs pass into the water with the faeces and are swallowed by
the fresh-water shrimp (Gammarus pulex). After hatching, the embryo
or acanthor penetrates into the body cavity or body tissues of the
intermediate host and there undergoes further development. After a
period of growth it finally becomes surrounded by a delicate cyst and
reaches the so-called infective stage, and is then known as an acan-
thella. If the shrimp is now swallowed by a duck or other suitable
host the worm is liberated from its cyst and develops to maturity in the
intestine of the bird.

The spiny-headed worms have developed a useful habit, namely the
power to re-encyst if ingested by an unsuitable host. If a crustacean
infected with the larva of a bird parasite is eaten, say by a small fish
instead of the "right" host, the worm is liberated in the intestine but
hurriedly penetrates into the tissues of the "wrong" host and becomes
re-encapsuled. Numerous transport hosts can be utilised and in this way
the worm's life is prolonged and its chances of reaching the "right"
host are increased. Possibly a new host may be found in the process,
in which development can take place. Sometimes a species like Centror-
hynchus aluconis which infests such birds as the tawny owl, little
owl and the buzzard passes from arthropod to frog, but may then
go on to small reptiles or small insectivorous mammals before reaching
the final host. In the case of the world-wide genus Corynosoma the
first host is an arthropod and the second a fish — but a series of the
latter may be interpolated before the final host is reached. Some
species, such as C tunitaey may be confined to sea birds — the gannet,
shag and cormorant — but others appear equally at home in marine
mammals and birds. For instance, C. striimosum has been recorded
from the grey seal (Halichoerus gryphus) from Carmarthenshire and in
the great northern diver from the Outer Hebrides. Further research
will probably show that these are closely related, though not the same
species.

The two acanthocephalids recorded from passerines in Britain are
Centrorhynchus teres from the jackdaw (a species mainly characteristic of
the Gorvidae) and Prosthorhynchus transversus from the starling, song-
thrush, blackbird and great spotted woodpecker. On the continent the
latter is found in a variety of hosts including the robin and nightingale.
There is also one record of Plagiorhynchus crassicollis jwhichis characteristic

igO FLEAS, FLUKES AND CUCKOOS

of waders, such as the ringed plover, Kentish plover, sanderling,
dunlin and oystercatchcr. It has also been recorded from the cuckoo.
At first sight it appears curious that the cuckoo should share a parasite
with this group of birds. On the other hand wagtails, which often act as
their foster parents, are infected with certain trematodes which other-
wise are chiefly found in waders. One can surmise that Crustacea form
a certain proportion of the wagtail's diet and the cuckoo may have
been fed the larvae as a nestling by its foster parents. Another species
found in waders in Britain is Arhythmorhynchus longicollis from the purple
sandpiper. It is also fairly common in gulls. Finally there is the
characteristic duck parasite Filicollis anatis recorded from the mallard
and scaup in Britain. It has a similar life history to P. boschadis^ using
hog slaters [Asellus aquaticus) as intermediate host. There are only two
species in this genus, one from Europe where it is also occasionally
found in moorhens and coots, and another from South America where
it parasitises gulls. In this genus the proboscis is bulbous and when
implanted in the intestinal wall of the host forms a powerful ball anchor
as the tissue of the host contracts round the narrow "neck" portion
below the bulb.

For such a small group acanthocephalids infect a really large variety
of birds. In 1933, Meyer listed over 300 host species, ranging from
penguins to eagles, and kingfishers to wood-warblers. The most heavily
afflicted family is the ducks (Anatidae), but waders, birds of prey and
thrushes are among the groups which are heavily attacked. The rock-
thrush which has a wide distribution in Asia, India, North Africa and
the Falaearctic region and has been recorded about eight times in
Britain, acts as an intermediate host for Echinorhynchus pachy acanthus,
which reaches maturity in predatory mammals such as the lynx {Felis
lynx) and jackal {Canis aureus).

The most impressive feature of an acanthocephalid is undoubtedly
the retractile proboscis (see Fig. 4 (3)) with which it anchors
itself to the host — for " it was all grown over with thorns."
These proboscis hooks are valuable characters for use in classifying the
whole group. In three of the four main orders, the spines are arranged
radially in long rows on the proboscis, but in the fourth order the
arrangement is in the form of a spiral. In two of these orders the trunk
spines are absent, but they are present in the others. They are also used
as aids for the diagnosis of lower categories such as the families, genera
and species. There are thin spines and stout spines, broad, long, stumpy.

WORMS igi

hooked, blunt, pointed, bent, curved and tapering spines. 1 hey vary
not only in shape, size, number and arrangement, but also in many
subtle ways such as the proportion of their different parts. A specialist
in the Acanthocephala must therefore resign himself to an endless
vista of measurements and the drawing of hundreds of little spines. We
have estimated that in one publication devoted to this group the author
has figured 12,000 spines.

Tapeworms (Cestoda)

Tapeworms, as Shipley pointed out, are like recurring decimals. At
one end there is a "head" or scolex, which is armed with hooks and
adhesive suckers and behind it stretches a long, pallid ribbon of seg-
ments which grow out from the "neck" region, each repeating the one
immediately behind it. Every segment (proglottid) carries a complete
set of organs, and it is, therefore, perhaps more accurate to think of a
tapeworm as a long chain of individuals joined together. However, the
nerve fibres and muscles extend through the whole length of the body,
so if the animal enjoyed any emotions they would be presumably of a
communal type.

Although the anterior or "neck" end is continuously producing
segments the tapeworm's length is limited, for at the posterior end the
oldest segments are dropping off — having gradually lost their initial
structure and degenerated into nothing more than bags of egg? which
pass out with the faeces of the host. During the course of its life one of
the large species of tapeworm has been known to produce seven kilo-
metres of segments.

Each proglottid carries a complete set of both male and female sex
organs, sometimes two of each. These are so arranged that each seg-
ment can fertilise itself but it is not unusual to find the different seg-
ments of a much coiled tapeworm having simultaneous sexual inter-
course at a number of points along its length. Everything, in fact, has
been sacrificed to communal egg laying, which, admittedly, is highly
successful but rather monotonous. One tapeworm has been calculated
to produce 36,000 eggs a day and up to two milliard during its entire
life.

Tapeworms have no alimentary canal and their food is absorbed
through the outer surface of the body. It has been suggested that during

192 FLEAS, FLUKES AND CUCKOOS

their early larval development the ectodermal covering is cast off and
that the endoderm which would normally form the alimentary canal
has taken over the duty of a body covering. It has further been suggested
that the entire adult tapeworm is an endodermal sac, the lumen of
which has been obliterated by the encroachments of the mesodermal
tissue. In this case it would be more correct to say that a tapeworm is
an alimentary canal without a body, rather than a worm without a
digestive tract.

The gut of vertebrates, which is the environment of all tapeworms,
presents certain unique features. To begin with it undergoes continual
peristaltic movement — that is to say rhythmical waves of contraction
pass along it. The tapeworm is continuously in danger of being swept
away — like a swimmer in a river with a powerful current forcing him
out to sea. The gut also contains protein, fat and carbohydrate splitting
enzymes and there is a wide range of pH. (1.7 in the stomach and 9.0
in the intestine). Moreover, the oxygen pressure is low and there are
regular physiological changes due to the feeding habits of the host.
Tapeworms have had to develop a series of adaptations to cope with
this particular situation. The cuticle of the cyclophyllidian cestodes
appears to possess a protective action which renders them immune to
digestion. Apparently no anti-enzyme is secreted. They have also
developed tolerance for a range of pH. varying between 4 and 11.
It has long been thought that cestodes were truly anaerobic and could
not make use of oxygen under any circumstances. Recently it has been
shown that, like roundworms and flukes, they will utilise it if it is
provided for them. In the gut, however, the most usual method is
anaerobic respiration.

In order to avoid digestion in the host's stomach the larval forms of
tapeworms have also become highly specialised in certain directions.
For example, if a cysticercus larva is swallowed by the final host the
scolcx is invaginated into a sort of sleeve which shields it from the action
of the gastric juices. The scolex only evaginates when it reaches the
duodenum and is stimulated by the presence of bile. The "sleeve"
which has received both the acid gastric juices of the stomach, and the
alkaline juices of the pancreas, is digested, but the scolex which has been
untouched by the former remains undigested and develops into a
strobila.

The health of the host and changes in its metabolism affect the
worms which parasitise it. In the laboratory it has been found that if

WORMS 193

the vitamin B complex is withheld from the diet of the host the tape-
worm produces no eggs but increases in size. On the other hand, lack
of vitamin B2 (vitamin G of some authors) in the diet of female rats
(but, curiously enough, not in males) causes their tapeworms to remain
undersized and stunted. Absence of carbohydrates in the diet and
possibly castration of the host, also inhibits their growth. In the labora-
tory it is frequently found that the host does not "do well" in captivity
and then the worms likewise appear in poor condition. All this goes to
emphasise a rather obvious fact that the relationship which exists
between worms and their hosts is both complicated and profoundly
intimate.

In one way, at any rate, cestodes are unique in the animal kingdom.
Their protein content is less than the sum of their glycogen and fat.

The tapeworms are certainly a very ancient group and they have
probably been committed to parasitism far longer than any of the other
flat worms, but their origins are lost in obscurity. There are no free-
living species, and apart from the egg, all the larval stages are endo-
parasitic — "they know not the light."

Birds must have undergone a great deal of their evolutionary
history accompanied by tapeworms as well as Mallophaga. They are,
therefore, a favourite subject with those systematists who try to demon-
strate the true relationship of the parasites and their hosts, by studying
them together. Krabbe first pointed out that each order of birds has
its own particular cestode fauna and that consequently these worms can
throw some light on the relationships of the birds. Over 900 cyclo-
phyllid tapeworms (ten families and 135 genera) are recorded from
avian hosts, and of the 45 known orders of birds 41 harbour " Taenias."
Baer has elaborated Krabbe's theory and obtained some interesting results
from his studies. Grebes and divers for instance harbour quite distinct
tapeworms and the fact strongly suggests that the two groups of birds
should not be placed together — as they often have been — in a natural
scheme of classification. Two genera, Schistotaenia and Tatria, are con-
fined entirely to grebes and, moreover, occur in this order all over the
world. The genera Gyrocelia and Progynotaenia are found in waders only.
Swallows and swifts each have distinct genera of tapeworms and
although they share Anomo taenia the species are different. This latter
genus is very large and spread through many orders, but certain species
are often characteristic of closely related species of birds which are
separated by wide geographical barriers. Thus, Anomotaenia constricta is

194 FLEAS, FLUKES AND CUCKOOS

found in Britain in the carrion-crow and the rook, and in the U.S.A., in
the eastern crow and the fish-crow {Corvus brachyrhynchos and C. ossifragus) .
From the same genus A. nymphaea occurs in the common curlew in
Britain and in the Esquimo curlew [Numenius borealis) in the U.S.A., and
A. arionis in sandpipers ( Tringa ochropus, T. stagnatilis and Actitis hypoleucos)
in Britain and in the yellowshanks ( T, jiavipes and T. melanoleuca) in
North America.

In another large genus Hymenolepis, which occurs in mammals as
well as birds, the same phenomenon can be observed, for species like
H. himantopodis occurs in Britain in the black-winged stilt {Himantopus
himantopus) and in the U.S.A. in the black-necked stilt (//. mexicanus).
Two other species of cestodes, Acoleus vaginatus and Diplophallus
polyniorphus are also shared by these two waders on both side of the
Atlantic.

The most impressive examples of this type are not, however, found
among the British fauna. A separate order has been erected for the
monstrously aberrant genus, Nematoparataema, which contains only two
species. One is found in the Australian black swan {Chenopis atrata) and
the other in the mute swan {Cygnus olor) in Sweden. The highly special-
ised genus Amabilia contains one species which is found in both African
and South American flamingoes. We have already noted on p. 145
that the African ostriches and South American rheas share the same
species of tapeworm, Houttuynia struthiocameli. It does not, in these
cases, seem unreasonable to suppose that when these hosts diverged
from a single stock they already harboured the tapeworms which are
still common to them both to-day. In the interval they themselves
have developed or evolved along different lines.

The Class is generally divided into two sub-classes, one of which is
reserved for the primitive Cestodaria from fish. The other, the Cestoda,
contains three orders, of which two infest birds. The first, the Pseudo-
phyllidea, develop as a so-called procercoid larva in the body cavity of
Crustacea, such as copepods, and in the plerocercoid stage in the
muscles and coelom offish. The sexual stage is found in aquatic and
fish-eating mammals, birds and reptiles. In the genus Diphyllobothrium
the final hosts include man, the cat, arctic fox, various seals, gulls, and
terns.

The great mass of bird cestodes are found in the second order, the
CyclophylHdea (Plate XXVIIc). These tapeworms are characterised
by the possession of four cup-shaped suckers on the scolex (see

WORMS 195

Fig. 4 (2)), often with a rostellum (or centre piece) armed with
hooks. Unhke the worms of the preceding order, only one inter-
mediate host is used apparently, by the cyclophyllids. The cysticercoid
larva generally develops in an invertebrate — an insect, mite, mollusc,
worm or crustacean. The adult is found in three of the main classes of
vertebrates, but principally in birds.

A glance at the cestode fauna of the domestic duck makes a conveni-
ent starting-point for studying many of the tapeworms of avian hosts.
One of the best known of the duck parasites of the order Pseudophyllidea
is Ligula intestinalis which has also been recorded in Britain from terns,
gulls, grebes, the shag, razorbill and crow. The first intermediate hosts
are the copepods Cyclops strenuus and Diaptomus gracilis. The second
intermediate hosts are fresh water fish which feed upon copepods,
principally bream, roach, dace, gudgeon (Cyprinidae) but also brook
trout, powan (Salmonidae), pike (Esocidae), perch (Percidae) and
lampern (Petromyzontidae).

The related genus Schistocephalus has similar habits. The first inter-
mediate hosts are various copepods {Cyclops viridus and C. serrulatus),
the second intermediate host is a fish, the miller's thumb {Coitus go bio),
the three-spined stickleback {Gasterosteus aculeatus) and the salmon {Salmo
salar), and the final hosts in addition to ducks, are divers, grebes,
guillemots, terns, gulls, auks and other aquatic birds.

Perhaps the most famihar of all the cyclophyUid tapeworms are
contained in the family Hymenolepidae. No less than fifteen species
of the enormous genus Hymenolepis have been recorded from the domestic
duck. The intermediate hosts of i/. anatina — which parasitises geese and
swan besides duck — are Ostracods {Cypria ophthalmica and allied species).
Other Hymenolepis develop in calanoid and cyclopoid copepods, fresh-
water shrimps {Gammarus) and water fleas (Daphnia). Insects serve
several species found in poultry and probably a similar type of inter-
mediate host is used by Hymenolepis parasitising tits, tree-creepers
nightingales and other small birds.

The common species Fimbriaria fasciolaris from the same family in-
fects a wide range of duck including mallard, teal, wigeon, garganey,
goldeneye, long-tailed duck, pochard, eider duck, scoters and mer-
gansers. The intermediate host is the copepod Diaptomus vulgaris.
Another allied genus is Aploparaksis, of which A.furcigera and one or two
other species occur in the domestic duck. Many wading birds are also
infected, and A. filum is common in the woodcock, jack snipe and

FFC— o

Fig. 4

Organs of attachment in three differeni
groups of internal parasites

(i) Proboscis of tongue-worm, Reig-
hardia sternae (x 5.5) from air sacs of
a tern, (after Heymons) ; (2) Suckers
and hooks of a duck tapeworm,
Hvmenolepis macracanthos (x 133),
(after Fuhrmann) ; (3) Proboscis of
spiny-headed worm, Corynosoma turbi-
dum (x 106) from a cormorant (after
Van Cleave)

WORMS 197

common snipe in Britain. Other species of the genus are found in gulls
and A. dujardini is a parasite of starUngs and thrushes.

A species of the genus Tetrabothrius is found in the eider duck, but
not in the domestic duck. This genus, which is a north European,
North American and Arctic group, is chiefly characteristic of sea birds,
such as the gulls and terns, but is also found in whales. In Britain
T, cylindraceus has been recorded from the manx shearwater, herring-
gull and fulmar, and T. macrocephalus from the red-throated diver, black-
throated diver and great crested grebe. One specimen of T. erostris was
collected from the glaucous gull.

An important family is the Davaineidae, which includes the large
genus Raillietina. These tapeworms are chiefly characteristic of the
orders Galliformes (gamebirds) and Golumbiformes (pigeons) although
several species, such as R. anatina, have been recorded from the duck, but
not yet from Britain. The known intermediate hosts include ants, flies,
beetles and snails. The same remarks apply to the allied genus Cotugnia.

Recently a great deal of attention has been centred on cestodes of
the family Anoplocephalidae, which are common parasites of mammal-
ian herbivores. One of the great mysteries of helminthology was solved
when Stunkard proved that the intermediate hosts of Moniezia are
oribatid mites, many of which live near the roots of the grass and are
accidentally ingested by the host while it is grazing. It will probably
be found that Aporina delafondi, which is a widely distributed parasite
of pigeons and turtle-doves in the Old World , has a similar life-
cycle.

Large numbers of hyper-parasites have been recorded from worms.
A book of over 450 pages has recently been published, compiled by
Dollfus, dealing exclusively with the parasites of helminths. Protozoa,
bacteria, fungi and other worms are the principal enemies. Generally
these organisms are mentioned in passing by the authors who are more
interested in the worms themselves. Birds must also rank as enemies, for
they search systematically for ripe proglottids containing eggs in the
faeces of animals and eat them with enthusiasm. We have already
mentioned that, at times, the sheath-bill {Chionis alba) subsists largely
upon the parasitic worms it finds in the faeces of colonial nesting birds,
particularly the gentoo penguins. As tapeworms require an inter-
mediate host for development the sheath-bills do not themselves
become infected, although they are continually ingesting millions of
ripe eggs.

ig8 FLEAS, FLUKES AND CUCKOOS

Flukes (Trematoda)

Bird flukes (class Trematoda, sub-class Digenea) are colourless, leaf-
shaped worms, generally only a few millimetres in length, which live
inside the various organs of the host's body. They feed on blood and

Dragonfly, Lihellula quadrimaculata,
an intermediate host of the oviduct fluke (x . 66)

lymph and other fluids and exudates and also possibly on cells of the
mucous membrane lining their particular habitat. They attach them-
selves by means of a sucker surrounding the mouth and also by a second
sucker when this is present, situated on the ventral surface of the body.
The reproductive system of flukes is fantastically complicated. Except
in one family, male and female organs are present in the same individual
and self-fertilisation is the rule. When a worm is preserved and stained
with various dyes, the different parts of the reproductive system can
be clearly seen forming intricate and gorgeous patterns. No
objective person can deny that the egg-shell producing glands of a
trematode worm are aesthetically satisfying. The excretory system is

WORMS 199

also very complicated, consisting of ramifying tubules with cilia
arranged at the terminal branches, which keep up a ceaseless flickering,
thus lashing the excretory products towards the bladder. These flame
cells are objects of great fascination — like candles twinkling on a
Christmas tree. On the other hand, the trematode's nervous system
is extremely simple and it has no blood circulatory system at all. Nor
does it possess a body cavity — so that the various organs lie embedded
in the fluke like currants in a cake.

Excellent habitats for the study of bird flukes are mud-flats and
saltings. These generally consist of flat stretches of mud and water, the
no-man's land of the countryside, treeless, colourless and desolate
expanses, which belong neither to sea nor earth. To those curious people
who are attracted by lonely communion with nature, the bitter-sweet
quality of these tidal deserts affords the acme of pleasure. There they
can really get their fill of pale sunshine mixed with the nostalgic cry of
curlews, and oyster-catchers twinkling against a skyline where sky and
sea merge into a melancholy glassy waste.

Saltings are a paradise for wild birds such as waders, ducks, geese
and gulls and for this reason they are also a paradise for flukes. The
conditions found in the pools on saltings are about as favourable as they
can be for these particular parasites; but the hazards of the trematode
life-cycle are so great that survival must always be problematical. The
future life for a larval flatworm is only the reward of one in a million.

A familiar bird in these surroundings is the redshank; and this is the
host of Cryptocotyle jejuna which, in the adult stage, is located in the
bird's intestine. The flukes' eggs pass out with the droppings and in
this way become scattered over the mud and in the brackish water
pools. Another animal which abounds in this habitat is a small mollusc,
one of the spire shells [Hydrobia ulvae). It is sometimes found in concentra-
tions of 32,000 to the square yard. The eggs of this particular redshank
fluke hatch if they are eaten by the snail in question. Whether they are
accidentally ingested with other food or whether Hydrobia has a fatal
weakness for trematode eggs is not known. Once inside the mollusc's
alimentary canal the Q^g liberates the ciliated larva known as a mira-
cidium. This quickly bores its way into the tissues of the snail. In
many species of trematode the miracidium hatches in the water and
actively seeks the snail host. These microscopical larvae are pro-
vided with eye-spots as well as a boring spine and swim vigorously by
means of their covering of cilia. They are generally strongly host-specific

200 FLEAS, FLUKES AND CUCKOOS

and will only attempt entry into the "right" host. Some molluscs, for
instance the scallops [Pecten)^ never harbour larval flukes, and appear to
be entirely immune to their attacks. Once inside the tissues of the snail-
host the miracidium degenerates into a hollow sac and a complicated
type of asexual multiplication follows, the exact nature of which is still
not understood. One theory supposes that the germ cells, which are car-
ried within the body of the miracidium, segment and subsequently
fragment; and these fragments give rise to the different types and differ-
ent generations of larvae which develop in the snail (germinal lineage
with polyembryony) . There are numerous other theories, none of which
is satisfactory. The larval form following the miracidium is an immobile
simple sac-like structure known as a mother sporocyst. The next
generation in the case of many species, including the redshank fluke,
are larvae of a more complicated type which are called rediae. These
are hollow worm-like forms, which possess a pharynx, primitive gut,
specialised secretory cells, excretory system, and an ambulatory process.
They are capable of a limited amount of movement, and feed actively
upon the tissues of the host. Within their body cavity daughter rediae
are developed, resembling the mother rediae, which emerge through a
birth pore and add to the population, feeding and growing in the
reproductive and digestive organs of the snail. Several of such genera-
tions are produced and then, for some reason not properly understood,
the germ cells dispersed in the bodies of the various rediae, give rise to a
different type of larva known as a cercaria. When these cercariae reach
a certain stage of development they emerge from the rediae and con-
tinue development in the tissues of the snail. Eventually they work
their way along certain well defined routes, such as the circulatory
system, and escape into the water.

The classical type of cercaria is similar in shape to the adult fluke
but provided with a tail. It does not remotely resemble the redia in
which it developed. Certain fundamental anatomical features — the
excretory system, suckers and gut — characteristic of the adult worm
can generally be observed in the cercaria. Many adaptations connected
with the free-swimming phase and the entry into the second inter-
mediate host, such as the tail, fins, eye-spots, penetration glands, boring
spines and cystogenous glands, are generally present.

In the case of the redshank fluke, thousands of cercariae emerge
from one spire shell — all the progeny of a single ^gg. They are just
visible to the naked eye, and, hanging motionless in the water, they

WORMS 201

resemble minims on a line of music. The body is a semi-transparent
colourless oval and the tail long and thin, and held aloft. The micro-
scope reveals that this tail is provided with undulating frilly fin-folds.
The cercariae of the redshank fluke can live in the water about eight
hours. They swim strongly for a few seconds and then stop suddenly
and sink slowly downwards in the characteristic "minim" attitude.
Then, with equal suddenness, they begin to swim again. These cer-
cariae, which have eye-spots, are extremely sensitive to change in light
and shadow — a quality which no doubt assists them in reacting to the
presence of second intermediate hosts, which in this case are fish — the
gobies. If a cercaria accidentally comes into close contact with one of
these fish it immediately attaches itself by means of the anterior spines,
casts off its tail, pours out the contents of the penetration glands which
soften the skin of the fish and quickly bores its way inside. It soon
comes to rest a Httle way beneath the scales and there forms a trans-
parent cyst. Within the cyst it undergoes further development in the
direction of the adult fluke, and larval specialisations, such as the eye-
spots and boring spine, are lost. In some species of goby the presence of
the metacercaria stimulates the host to produce pigment granules in
the skin. The hideous black spots covering the specimen on Plate VI lb
each mark the site of one cyst of Cryptocotyle.

As we have seen the numbers of these larvae emerging from a
Hydrobia which has eaten one trematode ^gg may run into several
thousands. Occasionally a fish swims into a large swarm and the
simultaneous penetration of great numbers of cercariae kills it. But
even in small pools which favour high infection rates — for then eggs,
larvae and hosts are all present in a small area and are more hkely to
make contact with one another — it is usual to find that individual fish
harbour only a few cysts. When one of these fish is eaten by a redshank
— and contrary to general behef redshank are very fond of small fish —
the digestive juices dissolve away the cyst wall and the young fluke is
liberated and continues its development in the intestine of the bird.
Thus the life-cycle is completed.

In this hfe-cycle there are at least seven distinct phases : o^gg, mira-
cidium, mother sporocyst, redia, free-swimming cercaria, encapsu-
lated metacercaria and sexually mature adult. This is characteristic of
most bird flukes although in some species variations occur. The
miracidium can have a free-swimming stage while in others it has none.
Again the redial generations may be missing and instead a succession

202 FLEAS, FLUKES AND CUCKOOS

of sporocysts give rise to other sporocysts and cercariae. Sometimes the
mother sporocyst is lacking and a mother redia develops directly within
the miracidium. At times the cercaria encysts in the first intermediate
host, in the open, on vegetation or on inanimate objects. In this way
only one intermediate host is involved, but in other cases an extra, third
intermediate host, may be added. Despite these variations the cycle is
fundamentally the same and one can trace the Ggg, miracidium,
redia/sporocyst, cercaria and metacercaria stages before the sexually
mature adult is developed. This is one of the most mysterious aspects
of the digenetic Trematoda. As a group they are highly host-specific
with regard to the first intermediate host, which is almost always a
snail, a fact which has led to the widespread belief that they were
originally parasites of molluscs before the evolution of vertebrates.
Why have all these flukes followed this same path, and why has none
remained parasitic on molluscs in the sexual phase ? This appears to
be one of the most puzzling phenomena in the whole field of helmin-
thology.

Cryptocotyle jejuna belongs to a large group of trematodes (Opisthor-
chioidea) which are all characterised by the same type of cercaria.
With one or two important exceptions they use fish — fresh water, salt
water or brackish water species — as the second intermediate host, and
the final host is thus, of necessity, a fish-eating animal. A related
species (C. lingua) parasitises the herring gull in Britain and many fish-
eating sea birds (Plate XXVIIa). The periwinkle serves as the first
host (Plate XXVIII) and various inshore fish like gobies [Gobius],
wrasse (Z^^rw^spp.), rockling {Onos spp.), blennies {Blennius spp.), and
butterfish {Pholis) as the second intermediate host (Fig 5).

On the saltings it is a familiar sight to see large flocks of geese feeding
in the distance. With field-glasses one can sometimes identify brent
geese pulling at the eel grass stranded in the shallows — a plant which
constitutes one of their staple items of diet. A careful examination of
the long ribbon-like leaves reveals that they are often beaded with
small, dark, hemispherical pearl-like cysts. This is the metacercarial
stage of the trematode Catatropis verrucosum which as an adult worm is
found in the caecum of various geese and ducks, such as the barnacle-
goose, pink-foot, sheld-duck, merganser and so forth. The first inter-
mediate host is Hydrobia ulvae. When the cercaria escapes from the
mollusc it immediately settles on the shell of the snail or some in-
animate object nearby and pours out a secretion from specialised

^^ swimming ^'"^^

Fig. 5

Life-cycle of the herring-gull fluke, Cryptocotyle lingua. This trematode

in its final stage is recorded from various gulls; different species oi

inshore fish serve as second intermediate host, but the first intermediate

is invariably the periwinkle. Littorinajittorea.

204 FLEAS, FLUKES AND CUCKOOS

cystogenous glands. This fluid rapidly hardens into an impermeable cyst
wall. As Hydrobia is found in large numbers feeding upon Z'^siera, the
larvae when they emerge frequently encyst on the plant itself. The geese
and ducks become infected by ingesting them along with the Z^siera or
by accidentally swallowing the minute snails which are encrusted with
Catatropis cysts.

A few gulls are always to be seen dipping into pools, fishing in
the httle gulhes on the saltings, or sitting in small flocks along the
edge of the water waiting for the turn of the tide (Plate XL). No
group of birds seems more heavily infested with worms and at least
twenty species of trematodes have been recorded from the black-headed
gull alone. One of the great groups of flukes, the Plagiorchioidea, is
well represented in the gulls. The larvae of these flukes develop in so-
called sporocysts — which are morphologically somewhat different from
rediae — and although there are many exceptions to the rule, the
majority employ arthropods as the second intermediate host. They have
trowel-shaped cercariae armed with a minute javelin-like stylet with
which they pierce the softer portions of the host's integument.

In the intestine of the black-headed gull and various other
crustacea-eaters such as dunlin, godwits, turnstones, sandpipers,
plovers, oystercatchers and curlews we find various flukes of the
family Microphallidae, which are characteristic of the saltings and the
shore. Several different species use Hydrobia and Littorina as the first
intermediate host and the shore crab {Carcinus maenas) and Gammarus
and other amphipods such as sand-hoppers as the second host. In the
case of Maritrema oocysta (formerly known as M. humile) the cercariae cut
short the complicated life-cycle, for they never emerge from Hydrobia,
but cast off their tails and their stylet and encyst within the snail. Thus
the redshank, which serves as the final host, becomes infected by eating
the mollusc.

Another group of plagiorchid trematodes which infests an incredible
variety of bird hosts are the oviduct flukes (Prosthogonimus) . These
worms have attracted a great deal of attention, for their presence in the
domestic fowl greatly reduces egg-laying. Sometimes they get caught
up in the egg during its development and any trematode the reader may
find cooked up with his breakfast is almost sure to be this species. Up
to date the known life-cycles all follow a similar pattern. The cercariae
emerge from a freshwater snail and swim about in the water. Accident-
ally they are drawn into the rectal respiratory chamber of a dragon-fly

WORMS 205

nymph. With the aid of their stylet they penetrate the integument and
later migrate into the muscles of the insect, eventually encysting in the
haemocoel. These metacercariae within their cyst are carried over
to the adult dragon-fly (see p. 198), when the insect under-
goes metamorphosis. Birds become infected by eating either the
nymph or perfect insect. On the saltings geese, gulls and duck are
frequently infected with P. ovatus, but this widespread fluke has been
recorded from such varied hosts as skuas, sparrows, guillemots, corn-
crakes, hawks and plovers. The only British record is from the crow,
although it must occur in many of our common species.

There is yet another large group of flukes, the Echinostomatoidea,
which is exceedingly common among the birds on the mud flats and
seashore. They are characterised by a collar of spines, which is generally
clearly visible in both cercaria and adult. The classical life-cycle for
echinostomes which infect birds, involves two molluscs — the first a
gastropod such as the winkle, whelk, top-shell, purple or spire-shell.
The second is often a bivalve (lameUibranch) Hke the cockle, mussel or
the clam. However, there are many variations and bird flukes of this
group can sometimes use the same species of snail as both first and
second intermediate host.

Many of the birds which frequent the mud flats and saltings are
winter visitors. In the spring and summer they seek other haunts and
during the breeding season they frequently become infected with flukes
which are confined to fresh water invertebrates as intermediate hosts,
and therefore, are not to be found in the larval stages on the mud flats.
Different species from many of the large groups of bird trematodes,
such as the Echinostomes, Notocotylids and Heterophyids, are adapted
to fresh water as well as marine and brackish water, but others, such as
the true fork-tailed cercariae, which are found as adults in mammals
and birds are restricted entirely to fresh water. Of these the blood
flukes (schistosomes) are the most notorious, for they have been a
scourge to man in semi-tropical and tropical countries at least since the
days of the Egyptian Pharaohs. In Britain there are no blood flukes
which parasitise human beings. Birds are less fortunate. The duck
mallard, teal, tufted duck and garganey — which form such attractive
little parties along the main channels on the saltings — frequently fall
victim to these worms on the stretches of fresh water they visit at other
times. The snail host of the bird blood flukes {Bilharziella, Gigantobil-
harzia, Trichobilharzia) are pond snails such as Limnaea and Planorbis,

2o6 FLEAS, FLUKES AND CUCKOOS

The fork-tailed cercariae escape into the water and after swimming
about either attach themselves to the surface film, pieces of floating
vegetation or each other, by means of their suckers and a slimy secre-
tion. Duck, gulls and grebes, which swim in the water, sometimes
come into contact with these cercariae, which by-pass the feathers,
quickly penetrate the skin and migrate into the abdominal veins of the

bird.

In the family Schistosomatidae the second intermediate host is dis-
pensed with; there is no encystment or metacercarial stage and the
cercariae penetrate directly into the final host. Another unusual
characteristic of the blood flukes is the fact that the sexes are separate.
Parthenogenesis has been recorded in one or two species. In some
genera the male is provided with a double flap of skin which forms a
ventral groove in which the female is carried about. In a permanent
embrace they move slowly against the flow of the blood stream, laying
their spined eggs as they go.

Not infrequently bird blood flukes attempt penetration of human
beings with whom they make contact in the water. Although they do
not undergo development in man, in the process of penetration they
produce a disagreeable urticaria, known as swimmer's itch.

The other large group of fresh water trematodes with which birds
on the saltings are frequently infected is the Strigeoidea. These are also
related to the blood flukes, but instead of simplifying the life-cycle by
omitting the second intermediate host, there is a tendency to complicate
matters by interpolating extra hosts. In the case of Cotylurus cornutus,
which inhabits the intestine of birds, the freshwater pond snails of the
genus Limnaea serve as the first host. The fork-tailed cercariae which
emerge into the water then penetrate other snails or leeches where they
develop into a special type of metacercaria known as a tetracotyle.
Swans, which somehow look vaguely out of place on saltings, and are
more at home on artificial lakes and ponds, are often infected. So are
duck, like scaup or mallard. Another strigeid, Apatemon gracilis, is
passed on to smew, mergansers, goldeneye, scoters and wigeon in
leeches. Gulls, such as the herring-gull, kittiwake, common gull, great
black-backed and black-headed gull, are frequently infected with
Diplostomum spathaceum, which is also located in the bird's intestine. The
first intermediate host is, once again, a pond snail of the genus Limnaea,
The second intermediate host is a freshwater fish, of which the rainbow
trout is the most generally favoured. When the fork-tailed cercariae

WORMS 207

have penetrated the skin they work their way through the flesh until
they reach the blood circulating system. Here they migrate along the
vessels until they reach the lens of the eye, where their peregrination
ends. They do not encyst but remain as so-called " Diplostomulum "
larvae which are free in the tissues of the host and there undergo further
development. The pressure of these larvae often causes blindness in
the infected fish and this probably furthers their chances of reaching
the final host.

A number of small passerine birds such as wagtails and pipits are
regularly seen on the saltings and although their flukes are principally
found encysted in insects, some of their characteristic trematodes are
essentially part of the brackish water fauna.

These few examples of the flukes found in a small number of repre-
sentative birds in a restricted habitat scarcely touch the fringe of the
subject, for trematodes are found in almost every species of birds and
in almost every organ of the bird's body — ranging from the eyeball and
frontal sinus to the air sacs, the kidneys, the stomach and the skin. In
their life-cycle they utilise a vast network of animals — molluscs, leeches,
worms, Crustacea, insects, amphibians, fish and even small mammals.

At first sight it appears that adult trematodes are not a suitable
group for studying the parallel evolution of host and parasite. It is,
of course, obvious that the links between certain hosts which harbour
similar worms, are their similar feeding habits, not hidden relationships.
The cat, bass, osprey and man are all parasitised by the superfamily
Opisthorchioidea — because they all eat fish. Frogs, bats and swallows,
because of their predilection for insects, are the victims of the Plagior-
chioidea. Nevertheless, once flukes become established within a certain
group of animals they begin to evolve parallel with their hosts and in
many cases it has been found that particular families of birds are
parasitised by certain sub-families and genera of worms. It is certain
that this particular line of research among trematodes will prove most
fruitful and that more profound studies will reveal far greater host
specificity, segregation and parallel evolution with the host, than is
suspected at present.

The solving of life-cycles, however, is probably the most interesting
and rewarding research in Helminthology to-day. The fluke living
under the eyelids of carrion-crows is a peculiarly interesting species —
but how does it get there ? That is considerably more interesting. In
order to solve this question one has to inquire into the habits of the

208 FLEAS, FLUKES AND CUCKOOS

crow and also, most probably, into the biology and ecology of almost
all the other animals with which the crow comes into contact. For
instance, one of the bivalves it eats on the saltings might be the inter-
mediate host: or the snails near the river : or one of the parasites which
infest its own body : or some larval insect it picks out of a puddle or
one of the mice it pounces on in the fields. Moreover, the linking of
adult worms with their larval forms often reveals their correct systematic
position and their relationship with other groups. Oddly enough,
research into bird trematode life-cycles is, in this country, as untouched
as the arctic snows. Anyone who cares to examine a few of the com-
moner brackish water molluscs can turn up a "new" undescribed
cercaria with an unknown life history every day of the year. Yet, at the
time of writing there is not one single worker in this field in Britain.

Leeches (Hirudinea)

Leeches belong to a much higher category of animals than the other
parasitic worms which attack birds. The Annelida are thought by
some zoologists to be in the direct line of descent of the vertebrates, for
they are metamerically segmented, possess a closed blood system and
paired primitive kidneys (nephridia) along each side of the body.

The majority of leeches are predatory and even the parasitic
species are only temporary parasites, adhering to mammals, birds, fish
and frogs long enough to gorge themselves on blood — rather after the
fashion of ticks and mosquitoes. The smallest of them, however, can
pierce epithelial surfaces and they have been found in a variety of
strange situations — on the gums of crocodiles, the lips of horses,
attached to man's tonsils, in the pouches of pelicans, the anus of ducks
and the trunks of elephants. The last fact impressed Pliny, who
remarked : " The beast is by their tickling and sucking in his snout
almost mad; which doth manifestly show the wonderful power of
insects; for what is there greater than an elephant ? and what is there
more despicable than a horse leech ? Yet the greatness and wit of the
elephant must give way and yield to this Worm."

The only important leech parasite of British birds is the duck leech
{Protoclepsis tesselata, fa-mily Glossiphomda.e), which has been recorded in
this country in ponds, and from the wigeon, teal and long-tailed duck
(see tail-piece Chapter X). It is quite often found adhering to the

WORMS 209

plumage of migrating birds and in this fashion must be carried far
afield. Leeches generally attack the mucous membrane of the head,
especially the nostrils, and domestic duck are not infrequently choked
by an accumulation in their trachea which thus blocks the air passages.
Leeches are also occasionally found in the digestive tract which they
gain via the vent. The odoriferous greasy secretion of the uropy-
gidial glands of water-birds is said to attract them strongly.

The duck leech, which is extremely active and restless, is quite small,
only about 16 mm. long and barely 2 mm. in width. It is a beautiful
olive green and pale grey in colour, finely sprinkled with black star-like
pigment spots. There is a sucker at each end of the body, although in
the preserved specimen figured on p. 210 only the large posterior disc
shows up clearly. The mouth is provided with a protractile sucking tube
which inflicts a small circular wound. Some leeches which have jaws arm-
ed with pointed teeth leave a wound like a three-pointed star. The
digestive system is highly developed. The stomach has an acid re-
action and is provided with voluminous caeca in which blood can be
stored almost unchanged for many months. This enables the leech to
undergo long periods of fast. The intestine has an alkaline reaction and
in some species is also provided with lateral expansions. Glands which
secrete a powerful anti-coagulant are situated in the head. It is this
secretion which inhibits the clotting of blood in the wound made by
leeches and which can thus be the cause of fatal haemorrhages in the
host.

The duck leech is hermaphrodite and after copulation and fertilisa-
tion both parties separate, lay eggs and rear young. They are admirable
parents, for not only do they brood their eggs but they also carry their
200-300 young about with them attached to their ventral surfaces.
The aquatic hirudinids as a group have many enemies and are preyed
upon by birds and mammals, frogs and newts and predatory insects
such as dragon-fly larvae and water beetles. On the other hand they
are carriers of various diseases of vertebrate animals ranging from a
fatal frog trypanosome to the virus of fowl-pox. They are also inter-
mediate hosts of several duck trematodes — a fact which demonstrates
how persistently they are eaten by these birds.

The medicinal leech (Hirudo medicinalis) is a much larger species and,
apart from other differences, has bright red blood, whereas that of the
duck leech is colourless. Despite the observations of Pliny the presence
of leeches is often quite unsuspected by their victims. Their bite is

2IO FLEAS, FLUKES AND CUCKOOS

painless and it is for this reason that they can obtain copious feeds
without attracting the host's attention. The medical profession, for
hundreds of years, used them for blood-letting and in this manner
claimed to cure innumerable diseases. Thomas MoufFet remarked that
"it were too tedious to reckon up all the melancholique and mad people
that have been cured by applying leeches to the Hemorrods in their
fundaments." Nevertheless, he was much impressed by the cure of the
noble Richard Cavendish. " Now to the great wonder of the court he
walks alone without help and being sound and void of all pain, he lives
an old man." It is of course impossible to know for certain if a duck is
tickled or worried by leeches attached to its vent, but it is unlikely
that their presence is in any way beneficial.

Duck leech, Protoclepsis tesselata,
from trachea of a teal (x 5.5)

■v..

"^vV\ ■ "•"•'•..X

n X

Plate XXIX

Arthur L. E. Barron

Biting midge, Culicoides obsoletus (female, x 57)

S. C. Porter

a. House-gnat, Culex pipiens, adult female
at rest ( x 5-8)

S. C. Porter
b. Aedes sp., adult female at rest ( x 5-8)

J. G. Bradbury J- ^ • Bradbury

c. Culex pipiens, larva ( x 9-5) d. Culex pipiens, egg raft ( x 14)

Plate XXX MOSQUITOES WHICH FEED OX BIRDS

CHAPTER I I

FLIES (DIPTERA)

All of them are begotten of filth and nastiness, to which they
most willingly cleave, and resort especially to such places
which are so unclean and filthy ; unquiet are they, importunate,
hateful, troublesome, tumultuous, bold, saucy.

Thomas Mouffet

Louse-Flies, Mosquitoes, Midges, Black-Flies,
House-Flies, Blue-Bottles and Nest-Flies

F WE could talk to birds as we talk to each other we would probably
find that flies loom very large in their lives and provide one of the
major topics of conversation. By day they form a favourite article of
diet for many birds, but during the night the tables are turned with a
vengeance. Incidentally it is an act of great cruelty to leave a canary
uncovered in a cage after dark, for it is then assailed by all the female
house-gnats, which, during the day, sit about silently on the walls and
ceiling of the room.

Flies are carriers of many diseases of both man and birds, and from
this angle are certainly the most important group of insects. They are
distinguished by the possession of only one pair of membranous wings
(which are lost in some parasitic forms), the second pair being represent-
ed by an insignificant pair of knobbed appendages (halteres) which the
ancient writers mistook for "eyes hanging by their sides." These can be
clearly seen on Plate XXIX. A fly's head is joined to its thorax by a
slender flexible neck. The various component parts of the thorax are
fused, and this again is joined to the body by a distinct waist. The
mouth parts of the various types of flies are profoundly modified accord-
ing to the food they eat (Plate XII, a and c) but most of the parasitic
forms are blood-suckers. The metamorphosis of all flies is complete,
that is to say they pass through an egg, larval and pupal stage before

FFC— P 2 1 1

212 FLEAS, FLUKES AND CUCKOOS

hatching into the perfect insect. The louse-flies and the tsetse fly
{Glossina morsitans) y an African species, which is known to attack birds as
well as mammals, are viviparous. An impressive character of most
Diptera — as well as many other insects — is the instinctive protection
they afford their offspring by selecting suitable spots for laying their
eggs or larvae. For instance the sheep bot-fly [Oestrus ovis) deposits her
young larvae on the wing, striking at the eyes and nostrils of sheep or
goats. Sometimes she makes a mistake and darts at the eyes of shep-
herds whose breath smells of sheep or goat's milk. Some black-flies
(Simuliidae) crawl beneath running water in order to lay eggs on
submerged vegetation. An even more extraordinary case is that of a
South American warble-fly {Dermatobia hominis) which sometimes
attacks turkeys, causing nodule-like warbles in the superficial layers of
the body in which the larvae develop. This fly captures a female
mosquito and attaches her eggs firmly to its abdomen. When the
mosquito, loaded with ripe eggs, alights on some warm blooded animal
to feed, the larvae — apparently activated by the heat — quickly emerge
and penetrate beneath the host's skin.

LOUSE-FLIES (HiPPOBOSCIDAE)

The most highly specialised parasitic flies attacking birds are the
louse-flies (Plate IX). As adults they live permanently on the body of
the host, feed on its blood and pupate in its nest. Compared with a
robin a louse-fly is very large. It is over a quarter of an inch in length
and a small bird with one or two of these insects creeping about in its
feathers can be compared to a man with a couple of large shore crabs
scuttling about in his underclothes.

Hippoboscids (which also attack mammals such as sheep, horses and
deer) display the classical specialisation for an ecto-parasitic life. Their
antennae are sunk in a groove and the mouth parts form a piercing
apparatus and a long, sheathed sucking proboscis. Their wings are
often reduced or absent. They are flattened dorso-ventrally with re-
markably tough leathery cuticles; their legs are large and muscular and
armed with formidable toothed claws. The whole integument is
covered with ugly backwardly projecting spines. They have also
developed an extremely efficient method of moving among feathers —
darting and scuttling about at a remarkable speed — and are extremely
difficult to catch on a living bird. This manner of progression is, in a

FLIES 213

subtle way, very characteristic and was well described in the Theatrum
Insectorum : " They never fly forward but sidelong, as it were,
hopping and skipping as they go. " For reasons which defy analysis,
louse-flies are particularly repellent insects, and most people experience
a shudder of disgust at the sight of them, and are filled with a quite un-
reasonable feeling of horror if they happen to dart up their sleeves or
into their hair while handling the host. A bite from a louse-fly, which
is neither dangerous nor painful, is an occupational risk and keepers on
grouse moors and members of the Edward Grey Institute of Field
Ornithology are among the few people who are bitten fairly often.
Louse-flies are too large to infest the host in great numbers, for a big
infestation would kill the bird.

The usual hazards of a parasite's life make special precautions for
the offspring necessary. Instead of laying large numbers of eggs
hippoboscids go to the other extreme. Only one young is produced at a
time but it is hatched and nourished within the body of the parent fly.
It is subsequently deposited in the nest as a fully grown larva which
immediately pupates. In this stage it passes the winter and hatches out
the following spring. The adult fly is also rather long lived and may
survive several months.

It has already been mentioned that some louse-flies have fully
developed wings and some have mere vestiges which are useless for
flight; in others again the wings are cast off when the fly reaches the
host. The sheep ked {Melophagus ovinus) has no wings at all (Plate IXc) .
It was pointed out in the chapter on evolution that it is a great advant-
age for a parasite which lives on the body of the host not to have wings.
In the case of birds such as the swallows and swifts which return year
after year to an old nest, the difficulty of finding a host is greatly
reduced. It is therefore not surprising to find that the wings of the swift
louse-fly {Crataerina pallida) and the swaflow louse-fly {Stenepieryx
hirundinis) are greatly reduced and non-functional (see Chapter 6). In
the case of the common louse-fly [Ornithomyia avicularia) which is found
on a wide variety of birds, ranging from robins to arctic skuas, the
difficulty of finding a host stifl sets a premium on wings, and they are
fully developed in this species.

In Britain there are five species of louse-fly known from avian hosts.
Apart from the three already mentioned, the finch louse-fly {Orni-
thomyia fringillina) is a common species (previously also known under
the name of 0. lagopodis) and is recorded from many hosts, and the

214 FLEAS, FLUKES AND CUCKOOS

heron louse-fly {Lynchia albipennis) was once taken off a purple heron.
In this country louse-flies are rarly if ever found on the bodies of birds
during the winter months but up to 50 per cent, of a population may
become infested in summer. The young are far more susceptible to
attack than adult birds.

It is interesting to find that the geographical distribution of some
species does not depend entirely on the distribution of the host. The
common louse-fly in Britain has a distinctly southern distribution;
faither north it is replaced by the grouse louse-fly. The two species,
however, are difficult to distinguish and are often confused; further
information is required before defining the exact areas they occupy.
Like the fleas, the bird louse-flies spend a part of their life-cycle in the
nest, so they are not entirely protected from changes in cHmate. This
factor is probably the key to their respective distributions.

Outside Britain a malaria-like parasite of birds [Haemoproteus] is
spread by the pigeon louse-fly (Pseudolynchia canariensis) . Since many
wild birds are infected with this disease in Britain it is highly probable
that our species of hippoboscids are also carriers of the disease.

Mosquitoes and Gnats (Guligidae)

Mosquitoes and gnats are smaU slender flies with long legs and an
elongated proboscis adapted for piercing and sucking (Plate XIIc).
If they are examined carefully the characteristic fringe of scales — often
rainbow-hued — on the veins and margin of the wings can be seen. " The
structure and make of the gnat," wrote one of the early naturalists,
"there is no man but may justly admire. For in that so small insect and
as good as none almost what reason is there ? what inextricable
perfection? . . . where his taste, where his smelhng? where is begotten
that terrible and great sound?" It nevertheless would have surprised
the writer to know how much print and paper has been devoted
to the mosquito since his day. Even the fall of the Roman
Empire has been seriously attributed to their agency, as carriers of
malaria.

Mosquitoes are a fairly large group of which over 2,000 species have
been described — about 30 from Britain. They are found throughout
the world from the tropics to the arctic circle. The most important
genus as far as birds are concerned is Culex, although some species of
Aedes and Anopheles, both found in this country, wiU sometimes attack

FLIES 215

birds. Culex is an ancient genus, which already existed, as the fossil
record proves, in the Oligocene period thirty million years ago. It is
now mainly tropical or subtropical, only a few species penetrating into
the temperate zone. Four of these are British, but only one, the most
common and familiar of all mosquitoes, \h&]io\i?>G-gndit {Culex pipiens),
is an important parasite of birds (Plate XXX). In India, Ross used
the related C. fatigans for his world famous experiments proving the
transmission of bird malaria by these insects.

Only the female house-gnat bites, and she does so principally at
night. It is when swallows and martins gather in the reeds in communal
roosts prior to migration (see Plate XXVI) that they are severely
attacked, and mass infection with bird malaria frequently follows. In
the southern seas these insects are said to cause entire colonies of pelicans
to desert their nests. The behaviour of mosquitoes in the dark is difficult
to observe unless they attack man himself, but recently an extremely
ingenious invention has made this task much easier. Large numbers of
the insect are captured and then sprayed with fine luminous adhesive
dust. Subsequently they are released and their movements can be
followed in the dark like aeroplanes with lights attached to their wings.
It is not known if roosting birds are frightened by the pipe of a female
mosquito. There is, however, some evidence that cattle have an in-
herited fear of the hum of the warble-fly {Hypoderma bovis) and an
inherited fear of gnats might well have survival value in birds.

Mosquitoes are as a rule very fussy about the conditions in which
they will mate. Some choose the evening before dark but only when
the light intensity has fallen below 2.0 foot-candles. A bright light
will put them off. As for the house gnat, it refuses to mate in a
confined space. If the air is still the males swarm, just after sunset and
again immediately after dawn, about six to nine feet from the ground
to the leeward of some prominent object, like a high hedge or the stone
coping on a roof. In the case of Culex pipiens about 50 to 100 males take
part and the whole swarm moves rhythmically up and down — in the
case of some other gnats it oscillates from side to side. The female is
attracted by the hum of the swaying column and in the excitement her
natural reserve is broken down and she is drawn into the swarm. She
is then seized by a male, and the couple drop out of the dance and
copulation takes place on the ground.

The house-gnat lays her eggs in the form of a boat-shaped raft which
floats (Plate XXXd). In order to do so she stands on the surface

t
2l6 FLEAS, FLUKES AND CUCKOOS

of the water, crosses her long hind legs near their extremities, and
extrudes her eggs which are covered with adhesive cement,
within the V-shaped mould thus formed. Each raft consists of
200 to 450 eggs and she may produce five or six rafts during her life.
Culex pipiens lays on clean or foul water, in butts and tubs, tanks, wells,
ditches, pond margins and stagnant puddles contaminated by farm
manure or urine. Eggs are also deposited in pools in salt marshes
providing they do not contain more than half sea-water.

Gnat larvae (Plate XXXc) are aquatic and sometimes occur in
vast numbers. It was once estimated that 400,000,000 were present in
two acres of Hampshire flood water, only a couple of inches deep. They
feed by whirling minute particles of food into their mouths by oscillating
a brush-hke moustache, or by chewing up vegetable or animal matter —
including one another if they get the chance. After moulting three
times the larva pupates. The pupa is also aquatic and, like the larva,
floats near the top of the water with its respiratory trumpets piercing
the surface film.

The males hatch first. During the summer they dance their lives
away and die when the cold weather sets in. Their mouthparts are
poorly developed and they cannot suck blood and are limited to a diet
of fruit juice and nectar. It is easy to distinguish a male from a female
mosquito without the aid of a microscope as the male has feathery
antennae. In the human species it is man that has a deep voice but in
gnats conditions are reversed and the pipe of the male is several notes
higher than that of its mate.

The female house-gnat requires a blood meal before she can lay
fertile eggs and her chief victims are birds, although she will occasion-
ally bite frogs and snakes and even mammals. In captivity her tgg output
is trebled if she is fed on bird's blood. Certain species ofAedes have been
known to migrate thirty miles inland from the saline marshes where
they breed, presumably in search of a blood meal. They subsequently
return to the marshes to lay eggs. The distance covered is known
accurately, owing to the re-capture of marked specimens. Culex pipiens
will also supplement her diet by feeding on nectar, milk standing in
pans, and even port wine. In the modern dairy the separator has
deprived them of their chief source of milk, as a thick layer of cream on
top appears to be an essential condition of feeding. Piercing the cream
to get at the hquid beneath seems a satisfactory substitute for piercing
the skin of a vertebrate animal to reach the blood below. When feeding

FLIES 217

on flowers she will also pierce the involucral bracts in order to get at the
honey. When the female is fully fed her voice drops in pitch from F to
D. She is a voracious feeder and will ingest 1.2 miUigrams of blood in
a single meal although her own weight is only 1.4 miUigrams. Small
wonder that her voice becomes a trifle mellow.

Unlike the male, the female house-gnat survives the winter by
hibernating in cellars, cool outhouses, dairies and cricket pavilions and
living upon her own fat-body which is a reservoir of food. If she mates
in the autumn she can store the sperm in her body and fertihse her
eggs in the spring.

In Part II it was shown that different species of bird fleas are
"zoned" according to the nesting habits of the host. Different species
of mosquitoes also frequent fairly well defined elevations — a fact which
is most noticeable when they swarm. Traps baited with living birds
reveal that different genera and species are caught near the ground, in
the lower and middle branches, and near the tops of trees. In nature
there is probably a closer link with definite species of bird host than has
hitherto been realised.

As carriers of disease female mosquitoes have no equal. Malaria,
yellow fever, dengue and filariasis are among the maladies transmitted to
man in the tropics. In Britain they transmit malaria and fowl-pox to
birds and probably also filaria. They themselves have many enemies.
Water-beetles, dragon-fly larvae, various small fish and newts feed
voraciously on the immature stages. In the course of nine nights one
newt ( Triton) ate no less than 985 gnat larvae. Bats and birds, especially
swallows and swifts, feed eagerly on the adults. Apart from one midge
which sucks blood directly from gorged female mosquitoes instead of
from the body of a mammahan host, they are free of insect parasites.
This is remarkable when we consider the vast number of species which
attack butterflies, moths, beetles and wasps, and so forth.

Naturally the best known parasite of the house-gnat is the malarial
Protozoan, Plasmodium relictum, and its alHes. Susceptibility to
malaria appears to be hereditary in C. pipiens, and some strains are
completely resistant. The egg production of infected females is greatly
reduced and in this manner, as well as in a variety of other ways, it has
a deleterious effect on the host. There are also numerous other fatal
and harmful parasites of both larva and adult, ranging from Protozoa
and Fungi to scarlet hydrachnid mites, so it must be admitted that
mosquitoes themselves are not without their troubles.

2l8 FLEAS, FLUKES AND CUCKOOS

Owing to its great economic importance the group as a whole has
been intensively worked, and a vast literature has grown up around it.
Unfortunately mosquitoes have proved difficult insects to study. Three
hundred years ago Thomas Mouffet summed up the situation satis-
factorily : " The distinction of gnats," he wrote, "is very perplex and
obscure and has puzzled all the philosophers."

Black-flies (Simuliidae)

The so-called black-flies, which are not always black, contrast with
mosquitoes in a number of ways. They are smaller and dumpy, with
short legs, and the female bites only by day. The larva and pupa, how-
ever, are similarly aquatic but they mostly inhabit swift running streams
with highly aerated water and not stagnant pools.

The group contains approximately 500 species of which about 20
are British. Unfortunately very little is known about their blood-
sucking habits in this country and much of the available information
comes from observations made on similar species abroad.

The majority of species of black-fly attack mammals, but some con-
fine their attention to birds, while a few bite both types of host indis-
criminately. The best known bird black-fly in Britain, which is confined
to the south and south-eastern parts of the country, is Simulium venustum.
It will swarm on the heads and rumps of sitting hens and turkeys and
drive them off their nests, and it will also force its way under the wings
of young birds and suck their blood — sometimes with fatal results. The
bite of the black-fly is much more painful than that of mosquitoes and
its saliva decidedly toxic. At times they are responsible for the death of
large numbers of cattle in eastern Europe. In America S. venustum is the
carrier of a malaria-like parasite {Leucocytozoon) of wild ducks which it
occasionally transmits to the domestic variety with fatal results.
Another species is the vector of an allied Protozoan from the turkey.
As Leucocytozoon is widespread among British wild birds (see p. 169) it is
highly probable that black-flies are also carriers in Britain.

Only the female black-fly bites. The males are smaller and easily
distinguished by their greatly enlarged eyes which almost meet on the
top of their heads. Whereas the male mosquitoes attract the females by
a communal dance, the male black-fly actively seeks his mate and is
thus frequently found on or near the host. In some cases copulation
takes place in nooks and crannies on the body of the mammal or bird

FLIES 219

concerned. The female requires a blood meal before she can lay fertile

eggs.

The eggs, which may number over 300, are deposited in jelly-like
masses on the edge of streams or scattered over the water. In some
cases the female skims above the surface laying an egg every time she
dips her abdomen into the stream, and again at other times she crawls
below the water to deposit her eggs on submerged vegetation and under
stones.

The larva, which moults six times, has a fan-like structure round its
mouth with which it sweeps minute organic particles down its throat.
In order to be able to withstand a strong current it is provided with a
posterior circlet of spines by which it can anchor itself in the upright
position to stones and plants. In some streams there are very large
numbers of these larvae. A count once revealed 734 to a square inch on
a submerged branch. When the upper reaches of a stream begin to dry
up, which often occurs in the case of swiftly running rills or rivulets, the
larvae of some species migrate downstream.

The pupa is enclosed in a sHpper-shaped silken cocoon spun by the
larva. When the fly is ready to emerge it uses a sort of Davis-escape
device. Air collects within the pupal skin until it finally bursts. The fly
is then carried to the surface in a bubble of air, without even getting its
feet wet — and darts away into the sunshine. Adult flies migrate many
miles from their breeding haunts, possibly helped by the wind.

Birds destroy large numbers of black-fly. Chickens for example eat
them greedily, and when they approach a barnyard fowl singly it is
always a toss-up which will feed on the other. Aquatic birds also gorge
on the larvae which they skim off submerged vegetation and stones.

Mosquitoes are carriers of various species of Filaria — nematodes
which complete part of their development in the insect. Black-fly are
also carriers of a related group of worms. Onchocerca. The larvae of these
worms are confined to the connective tissues just under the skin of the
infested mammal. They are consequently taken up by Simuliidae,
which do not drill straight into the blood stream like mosquitoes but
rasp a hole in the skin of the host. It has been claimed that the saliva
of the black-fly attracts the worms.

Apart from Protozoa and nematodes there are several other para-
sites of these insects, but few, if any, are yet recorded from this country.

Although Simulium venustum is the best known of the bird black-flies
in Britain, there are at least two other species, .S*. latipes and S. aureum,

220 FLEAS, FLUKES AND CUCKOOS

which are far commoner and are distributed throughout England and
Scotland. King Lear may have had the latter species in mind when he
spoke of "the small gilded fly." The body of the female is covered in
dense, gleaming, golden scaly hairs, and on the wing it resembles a
little ball of light. It sucks the blood of geese.

Biting Midges (Geratopogonidae)

Midges suck the juices of flowers and pierce the wing- veins of dragon-
flies, butterflies, moths and lace-wings, and many small insects are
caught and devoured whole. One British genus only, Culicoides (Plate
XXIX), of which some thirty species are found in this country, feeds on
the blood of mammals and birds. The development of the parasitic
habit in this family is therefore particularly easy to follow. Relatively
little, however, is known about them or their life histories.

Midges are minute flies, only a few millimetres in length. The female
alone sucks blood — generally at dusk or by night, but sometimes in
blazing sunshine. The eggs are laid on moist soil or near water and the
larva and pupa are aquatic or live in damp soil. Unlike those of gnats
they can survive quite long periods out of the water without suflering
any ill effects. Sometimes they breed in the liquid running from manure
heaps, the sap seeping from gashes in trees or moist decaying
vegetable matter. One Japanese midge which attacks hens, breeds in
their dung.

There are no definite records of Culicoides biting birds in Britain
although it is fairly certain that most of the species do so. In the United
States large numbers of C. biguttatus^ closely related to C. fascipennis,
were found gorged with blood in the nests of crows and magpies.
Although they are so small, midges are cruel and persistent biters.
They do not fly in the wind, but they can soon take the romance out of
a still summer evening. C. impunctatus is a major pest in the west of
Scotland, "where its presence in conjunction with the kilt is said to have
given rise to the Highland Fling."

House-flies (Muscidae), Blue-bottles (Calliphoridae)
AND Nest-flies (Carnidae)

Most of the house-fly group are not blood suckers, but the African
tsetse flies (Glossina) attack both mammals and birds. The stable-fly

FLIES 221

{Stomoxys calcitrans), which is widely distributed throughout the British
Isles, is also occasionally found in birds' nests, and it is quite possible that
if no mammals are available it finds sparrows and swallows satisfactory
substitutes. The greatest numbers of the house-fly group, which are
found either as obhgate or occasional occupants of birds' nests, prey in
the larval stage on other dipterous larvae or eat decaying animal and
vegetable matter. They are not parasites of the birds themselves. The
majority of the blue-botde group are also parasitic in their larval
stages on the larva and pupa of other insects. Many breed in decaying
animal matter and sometimes they eat flesh and corpses. The larvae
of flesh-flies {Sarcophaga) and the green-bottles and blue-botdes [Lucilia
and Calliphora) and certain other genera are quite often found con-
suming the decomposing flesh in wounds on the bodies of birds. The
original wound may have been inflicted by a blood-sucking insect.
They are facultative parasites, and their presence is in the nature of a
recurring accident. One genus however, the blue or green metallic
flies {Protocalliphora), are true ecto-parasites of birds in the larval stage.

The bird-bottle fly (P. azurea) feeds on nectar as an adult, and it can
sometimes be seen around flowers in the sunshine (see tail-piece
p. 5). The larvae live in the nest and at certain intervals attach
themselves to the nestlings by their anterior end, which is modified to
form a sucker with hooks in the centre. Although they somedmes kill
the host they are frequently present in large numbers without apparent-
ly causing much harm. In one magpie's nest 373 larvae were counted,
but the fledgelings seemed healthy. The species is quite common in
Britain and has been recorded from a large number of birds, including
the nightingale, redstart, skylark, meadow-pipit, and various tits,
wagtails, crows, swallows and martins.

A frequent parasite of British birds with similar habits is the nest-
fly {Neottiophilum praeustum). It is a large yellowish brown fly and the
larva, which lurks in the lining of the nest, is a voracious blood-sucker.
The anterior end is armed with two strong hooks which it thrusts into
the flesh of the young bird while feeding. When fully gorged it drops
back into the nest. Too many larvae in one nest kiU the fledgelings and
the female fly guards against this disaster by dispersing her eggs in
several nests. The principal hosts are passerine birds and Basden has
reared it commonly from nests of blackbirds, thrushes, finches, warblers,
carrion-crow and the linnet ; but it has also been taken occasionally from
nests of the nighdngale, tree-creeper, sparrow and hedge-sparrow.

222 FLEAS, FLUKES AND CUCKOOS

One of the most interesting flies parasitising birds is Camus hemap-
terus. It is a tiny, shining, black-bodied fly, only a few millimetres in
length and it lives among the feathers of the host. The life-cycle is
passed in the nest. The larva (according to Nordberg) is saprophagous
and feeds on dead and decaying animal matter. Up to a few years ago
it was thought that the adult was a blood-sucker, but the mouth-parts
are not adapted for piercing and sucking and it is now considered more
probable that it feeds on the fatty or waxy exudates from growing
feathers. Both sexes of the fly are fully winged when they hatch, but
after reaching a host — even if the distance covered is a few inches from
the bottom of the nest to the back of a nestling — they break off their own
wings, some distance from the base where there is a line of weakness,
leaving a stump. After the wings are shed the abdomen becomes
enormously distended owing to the abnormal growth of the fatty tissues.
This curious condition is known as physogastry and it is usually devel-
oped by flies and beetles which are parasitic or symbiotic in ants' or
termites'nests.

Camus hemaptems has a wide distribution in Europe and America.
Host-selection seems to depend on the type of nesting site rather than
the species of bird. Tits, starlings, woodpeckers, and other hole-nesters are
greatly favoured, but a wide range of host records exists which includes
falcons, finches, warblers, crows, pigeons and swallows. It is not a com-
mon species in this country, although it is probably often overlooked,
and has been bred from the nests of the starling, hedge-sparrow, barn-
owl and blackbird. There are numbers of British species from the allied
genus Meoneura, all of which are very small flies about one mm. in
length. Sand-martins appear to be the host of M. lamellata, and a great
variety of birds harbour M. neottiophila in their nests, including hawks,
tits, woodpeckers, pigeons, finches, blackbirds, and carrion-crows.

The bird itself is an important enemy of flies but the various para-
sites which attack them are more important, especially in the larval
stages. One type of mite eats the eggs of Muscidae, the adults hitch-
hiking around on the body of the fly. There is also a formidable list of
Protozoa (including the trypanosomes) and Fungi, of which flies are the
known host. An exceptionally large number of pathological organisms
are associated with Diptera owing to their unsavoury habits. Thus
while feeding upon the excrement of birds they swallow the spores of
Coccidia, the causative agent of so-called grouse disease, which is thus
spread to other individual birds. They also swallow the eggs of tape-

FLIES 223

worms of birds and disseminate them far and wide. Moreover they
carry a truly remarkable number of bacteria about with them. Pains-
taking Chinese workers calculated the grand total from a single house-
fly and found 3,500,000 adhering to the outside and 30,000,000 to the
inside of its body.

Parasitic larva of bot-fly, Hypoderma bovis, (x 3 . 5)

CHAPTER 12

MITES (AGARINA)

They are so small that Epicurus said it was not made of
Atoms but was an Atom itself . . .

Thomas Mouffet

THE MAJORITY of mitcs havc roughly globular bodies, with their head
and thorax fused, two pairs of mouth-parts and four pairs of legs in
the adult stage. The larvae have only six legs when they hatch, but after
a certain number of moults develop into nymphs with the full comple-
ment of legs. They are so small that it is necessary to have recourse to
the microscope in order to see their structure. The number of species of
free-living mites only outnumbers the parasitic mites by about three to
one, and it is believed that parasitism must have arisen independently
about a dozen times in the group. If ever an assembly of animals were
pre-adapted to this particular mode of life it is the mites, not only on
account of their minute size and varied feeding habits, but also because
of their insatiable desire to wander about and creep into cracks and
crevices. Except in a few families they are not greatly changed by their
dependent existences. Mites living as ecto-parasites, however, even in
distantly related suborders, develop striated cuticles. This is another
case of parallel evolution which, like the development of combs on
insects, appears to be the direct result of life in fur and feathers.

The best known group parasitising birds is that of the red mites
(Dermanyssidae) which hide and breed in nests and under the bark of
trees and creep out at night to suck the blood of the host. A common
species in Britain is the swallow red mite [Dermanyssus hirundinis) which
greatly resembles the common red mite of poultry {Dermanyssus gal liriae),
also widely distributed in the nests of many wild birds, including various
passerines, gulls, and pigeons. D. quintus is a parasite confined to the
green woodpecker, and D.passerinus from the greenfinch is an interesting

224

MITES 225

Irish record. All the red mites are true blood-suckers and when present
in large numbers they may bleed the host to death. They are also
carriers of relapsing fever of birds. Fonsecaonyssus sylvarum, also a type of
red mite (Macronyssidae) which attacks poultry, pigeons and wild
birds, has been found to be naturally infected with the virus of western
equine encephalitis. Another related group sucks the blood in the nasal
cavities of birds, such as sparrows, bullfinches, swallows, dippers, eider
ducks and so forth. There are records from the Shetland Isles of
Rhinonyssus neglectus from the purple sandpiper, S terms tomum cale-
donicum from the guillemot and S. waterstoni from the little auk, and
several related species from various hosts.

Among the true feather mites the Analgesidae are the most familiar
on birds, and over 150 species are known from Britain alone. These
mites are not blood-suckers but feed upon the horny layers of the skin
and the feathers. Some genera are found exclusively on the pinions
(rectrices) of relatively large birds. Two well known examples are
Pterolichus ardeae on the heron and P. cuculi from the cuckoo. Occasion-
ally a species favours a circumscribed area of the pinions, such as the
white portions of the wings of the nightjar, and is not to be found any-
where else. Certain other genera, notably Syringobia from various
waders, including the sanderling and green sandpiper, and Thecarthra
also, from plovers and gulls, inhabit the quills of some of the larger
feathers and feed upon the pith. They seem to know when the moult is
due, for they are never found in cast feathers. They lay their eggs in
neat spirals inside the quill and if no male happens to be in the same
feather with the females, they resort to virgin birth. The genus Analges
and its allies contain mites which are found on all parts of the bird's
plumage except the pinions. The specimen of ^. chelopus illustrated on
Plate XXXIb, was taken from the hedge-sparrow. The enormously
enlarged third pair of legs of the male is a characteristic feature of these
mites. They are not used for fighting but serve to lock the female in a
firm embrace during copulation. In some species such as Megninia
strigis-otis from the short-eared owl the male seems to stimulate the
female by making passes over her with his huge legs and does not resort
to force. In other cases (such as Protalges attenuatus from the barn-owl)
his fierce love-making permanently dents her cuticle. These mites
normally copulate precociously, before they are mature. If no female
is available they pay a high price for their enforced virginity, for
development is retarded or even arrested, and they fail to grow their

226 FLEAS, FLUKES AND CUCKOOS

magnificent clasping legs — symbol of masculine virility in the acarine
world. Another group of genera is found on the feathers of the wings,
flanks and back of passerine birds. Some are confined to a single host
and others occur on a wide variety, but the majority favour certain
definite families and groups of birds such as finches, tits, crows or
thrushes. Typical British species are Trouessartia minutipes which is
peculiar to the house-martin, Joubertia microphyllus (Plate XXXIa)
which is found on the chaffinch and tits, and Proctophyllodes glandarius
which occurs on a wide range of hosts.

Certain wing mites [Oustaletia pegasus) found in the tropics on the
hornbills (Bucerotidae) have the dorsal setae modified to form feather-
like expansions. A superficial glance conveys the impression that they
are winged, hence their Greek name.

Members of another group of the feather mites live next to the skin
of the bird, at the base of the fine down feathers, and probably feed on
scurf and skin debris. Microlichus avus from the jay and sparrow and
Epidermoptes bilobatus from the fowl are typical examples.

Although all true feather mites lay their eggs on the feathers, in
some genera and species such as Falculifer rostratus from doves and
pigeons and Pterolichus obtusus from the partridge, the second nymphal
stage is passed in the fatty tissues beneath the skin of the bird. In the
case of Michaelichus bassani from the gannet, the membranes lining the
subcutaneous air-cells are selected, where the mite is often present in
large numbers. The males of this species are generally asymmetrical;
the only "normal" specimens have been found by Turk on gannets
from Great Saltee Island.

Closely related to the itch mites are the lung mites (Cytolichiidae)
which are found in the bronchial tubes and lungs of birds. Sometimes
they invade the air sacs and even bone cavities in such numbers that the
birds die of suffocation. Well known species in Britain are Cytodites nudus
from the pheasant and turkey and Laminosioptes cysticola from poultry.

The true itch mites (Sarcoptidae) are best known as parasites of men
and dogs and are the direct cause of scabies and mange, but some
species also attack birds. Thomas Mouffet described them vividly,
*' always lying under the outward skin and creep under it as Moles do,
biting it and causing a fierce itching." Familiar itch mites are the
species which cause scaly leg and de-pluming mange in poultry,
Cnemidocoptes mutans (see p. 228) and C. gallinae. As they pass their
whole life beneath the skin they have no use for the adhesive

«W)

•S

"rt

Arthur L. E. Barron

a. Nymph, ventral surface ( x i6)

W. T. Tarns H'- T. Tarns

b. Engorged adult from head of a willow-warbler, ( x 5-1), ventral surface and

dorsal surface

PlaU XXXII

THE SHEEP TICK, Ixodes ricinus

MITES 227

suckers on their feet, or the long tactile hairs which are characteristic of
most ectoparasitic mites, and these structures are missing in Cnemi-
docoptes. In addition their legs are very reduced and the mouth-
parts greatly modified.

An interesting family of mites is the Gheletidae, members of which
are predacious and hunt the true feather mites in the bird's plumage.
Some have abandoned this symbiotic way of life and have turned para-
site. The species of the genus Syringophylus live inside the quills of pigeons
and poultry and their bodies have become greatly elongated and pro-
foundly modified in shape to suit their long narrow habitat. In this
way they resemble the quill mites of the Analgesidae, which are also
slim and elongated. The quite unrelated and abundant hair-follicle
mites (Demodicidae), which are parasites of mammals, show a similar
type of adaptation; they have long cylindrical bodies and their legs are
reduced to mere stumps.

The genus Harpyrynchus is also truly parasitic. They live in the
feather follicles of passerine birds which they enlarge to form tumours
about the size of peas. These are located chiefly on the flanks and
wings of the host. The females never emerge from these tumours and
only the immature stages are "free". In shape they form a great con-
trast to Syringophylus. Far from being long and narrow they are almost
circular with stumpy legs reminiscent of the itch mites. Sometimes
colonies of Harpyrynchus destroy the follicular bulbs over large areas of
the birds' bodies, thus causing a sort of feather mange.

The Laelaptidae are essentially parasites of mammals, especially the
small rodents, but a few species are found upon birds. Eulaelaps novus
appears to be confined to the sand-martin, and Ptilonyssus nudus is
recorded from the song thrush and various small passerines in Britain.

The brilliantly coloured harvest mites (Trombidiidae) are parasitic
in the larval stages although free-living and predacious as adults and
nymphs. They are often found in great numbers on game-birds,
thrushes and other ground-loving species. They attach themselves to
the skin, which they pierce, and feed on lymph.

Mites of the family Tyroglyphidae, known as cheese mites owing to
their predilection for that particular delicacy, are often found in birds'
nests. They feed chiefly on decaying organic matter, but some are
predatory or parasitic. During development many species pass through
a dispersal stage known as a "hypopus nymph". The tgg hatches as
usual into a six-legged larva, which in turn sheds its skin and becomes

FFC— Q

228

FLEAS, FLUKES AND CUCKOOS

an eight-legged nymph. At this stage the subsequent moult produces
the hypopus. This form is devoid of mouth parts and cannot feed. The
legs are reduced and several adhesive discs or suckers are developed on
the ventral surface. It is solely adapted to phoresy or passive dispersal
by some arthropod carrier. It is these hypopus nymphs which are
found hitch-hiking on fleas (see p. 103), flies, ticks and even on the wings
of moths. They are never parasitic at this stage and use the adult insect
merely as a means of transport. Nevertheless in large numbers they can
cause the death of the transport host.

In the adult form the bodies and secretions of mites are toxic, at any
rate to man, and possibly to other animals. So-called grocer's itch and
miller's itch are really forms of acute dermatitis (sometimes accom-
panied by fever, asthma, vomiting and other symptoms) produced by
contact with flour and grain heavily infested with mites.

Itch mite, Cnemidocoptes mutans, occurring on various birds

(x 176)

MITES 229

Ticks (Ixodoidea)

Ticks are really only large mites which may reach a length of half
an inch or more when gorged. There ^re about 300 different species in
the world and as a group they are not really successful. Sometimes,
however, a single species is present in fairly large numbers. It was
estimated that in certain parts of the U.S.A. there were 2,800,000
feeding ticks to the square mile, parasitizing the snow-shoe hare and
ruffed grouse, but this is nothing compared with certain mites which
may number several thousand to the square inch.

A few species are confined exclusively to birds, although a fairly
high proportion feed on both mammals and birds and in their larval
stages some regularly attack ground-nesters, such as larks and plovers.

There are two groups of ticks which have adopted rather different
types of lives. Members of the family Argasidae, which are tough and
leathery with gorgeously embossed integuments, live and breed in
nests and burrows, and feed at night when the bird or mammal returns
to rest. They engorge very rapidly and therefore do not have to leave
the habitation of the host. They are found mostly in warm and tropical
countries and in the rigours of the British climate they seek out a species
like the domestic pigeon, which lives in sheltered dove-cotes. Members
of the other family of ticks, the Ixodidae, which have a dorsal plate or
scutum on their backs, are not nest dwellers and depend for food on a
chance meeting with the host as it wanders about in the fields and woods.
They engorge slowly and therefore spend a considerable amount of
time actually attached to the bird's body. The fully fed female of the
most famihar British species, the sheep tick, /. ricinus (Plate XXXII)
looks like a shiny blue pea sticking firmly to the skin of the host. The
mouth-parts are deeply embedded in the flesh and on account of the
recurved spines (Plate Xlld) which anchor the rostrum in position it is
extremely difficult to dislodge. This a typical adaptation to the para-
sitic mode of hfe and impressed the early naturalists. Thomas MoufTet
wrote, '' For Tykes will sometimes enter deep into the skin with their
nose, that you can hardly pull them out but with the loss of their heads
and they seldom wander but they bite cruelly and make themselves a
hollow place and there they stand fast." In addition to the spined
rostrum (Plate XI Id), ticks have suckers between their claws which
assist them in clinging to the host, especially before they become
fixed and in their larval stages.

230 FLEAS, FLUKES AND CUCKOOS

The lives of the Ixodidae are far more precarious than those of the
Argasidae — a fact which is reflected in their greatly increased egg out-
put, the females laying in thousands instead of hundreds.

Ticks are the great exponents of the gentle art of waiting. An adult
can wait from four to seven years for a meal and even a young larva will
survive six months without feeding. The great food reservoirs (for the
host's blood) in their branching intestines makes this extraordinary
endurance feat possible. Both sexes sometimes wait many months for a
mate and finally when they come together copulation can last over a week.

On emerging from the egg the larva has only six legs and is known
as a seed tick. It has to wait for a passing host in order to obtain the
first blood meal. Subsequently it drops to the ground or back into the
nest and moults into an eight-legged nymph. Again it has to wait for
the host and another blood meal, after which it once more drops to
the ground and moults, this time emerging as a fully mature tick
(Plate XXXIIb). Yet another wait for the host follows.

The familiar sheep tick {Ixodes ricinus), feeds equally well on a large
variety of mammals including stoats, red deer, rabbits, squirrels, mice
and even hibernating hedgehogs. In fact it will attack any warm-
blooded animal with which it comes into contact. It has been recorded
from many birds, and favours ground-feeding and ground-nesting
species like grouse, larks and meadow-pipits, but it has also been taken
from the long-eared owl, whinchat, redwing, blackbird, rook, lapwing,
chaffinch — altogether from 47 different British birds.

It is generally located on the head of an avian host, attached near
the eye or the angle of the mandibles, where it cannot be pecked off.
After engorging for a few days on the bird the female drops off to lay
her eggs, but an unfertilised female is incapable of finishing her meal
and remains attached, sometimes for weeks and months until found by
the male, who quickly puts an end to her dreary repast.

Copulation between ticks is most peculiar. The male enlarges the
female sex orifice with his rostrum — a surgical operation which takes a
considerable time — and then with the aid of his mouth-parts introduces
a packet of his own sperm inside the female. Soon afterwards he dies.

In most Ixodidae it is the male which actively seeks the female, but
sometimes the roles are reversed. Again there are those curious cases
where no male has ever been found and the eggs develop partheno-
genetically. In rare instances the males, which are dwarfed, are parasitic
upon the females, and suck the host's blood via the body of their mates.

MITES 231

There are several Ixodes which are confined to birds. A cosmopoHtan
species, widely distributed in the nests of sea birds is the guillemot tick
(/. uriae). In Britain it is recorded from gannets, fulmars, guillemots,
puffins, curlews and so forth, from many coastal districts including
Devon, Yorkshire, the Fame Islands, St. Kilda and Shetland. On a
narrow ledge of cliff 400 feet above the sea and frequented during the
breeding season by tens of thousands of sea birds, Hewitt observed a
pair of/, uriae copulating beneath a stone, with four or five males stand-
ing by waiting their turn. The scene was described in a graphic
correspondence with Wheeler at the end of the last century, and makes
the reader sigh for the days when naturalists still found time to cultivate
letter writing as an art.

Another species which parasitises sea birds is the shag tick (/. uni-
cavatus) which is confined to cormorants and shags and has been collected
near Plymouth, the Scilly Isles, the Cheddar Gorge and also certain
locations in Scotland and Ireland. /. canisuga is taken constantly from
the nest of the sand-martin in Britain, and continental writers consider
it is a separate species confined to this bird. Occasional records from
other bird hosts include /. caledonicus from crows, ravens, rock-doves and
a Greenland falcon from Scotland; /. brunneus, which is confined to bird
hosts in Europe, Africa and North America, and has been found once
in England on an owl ; and /. passericola which was discovered by Turk
on a Cornish house-sparrow nesting under the eaves of his own house.
There is also one record of Haemaphysalis cinnabarina from the stone-
curlew, and Hyalomma marginatum taken off a migrating rose-coloured
pastor on Fair Isle.

It is interesting to note that in the U.S.A. when the numbers of the
snow-shoe hares are at low ebb the tick population of H, leporis-palustris
depends almost entirely on the ruffed grouse [Bonasa umbellus) as an
alternative host.

The best known British example of the Argasidae, is the pigeon
tick [Argas reflexus). It lives in dove-cotes and pigeon lofts, although the
first record in this country was made from specimens caught in Canter-
bury Cathedral. At one time it was considered peculiar to "the dark
recesses of this time honoured fane." When pigeons are not available it
attacks other birds, such as sparrows and chickens.

Ticks are very dangerous parasites. Their saliva which they pour
into the flesh of the host can be highly toxic, and the bite of one tick
may kill the host. Even their eggs contain poisonous substances which

232 FLEAS, FLUKES AND CUCKOOS

can prove fatal to birds. Blindness sometimes follows attachment in the
region of the eye, and the flesh of the bird becomes "pulpy" and semi-
liquid in the immediate vicinity of the tick. Many fatal diseases of
mammals are carried by ticks and both the pigeon tick and fowl tick
{A. persicus) are vectors of fowl relapsing fever. The causative agent is
a spirochaete {Borrelia anserinum), which undergoes development in the
body cells of the tick. Many birds are susceptible to this fatal disease
which is passed on in the eggs of the tick. The larvae are thus already
infected at birth.

Some birds, besides the "delousers" mentioned in Chapter 3
destroy large numbers of ticks. Jackdaws have been seen feeding
avidly on the guillemot tick and in many places chickens are run
in with cattle and sheep to keep the pastures free of them. They are
also eaten by ants and are parasitised by small Hymenoptera which lay
their eggs in the bodies of young nymphs which are then consumed
alive by the developing insects.

Tongue-Worms (Pentastomida)

The tongue-worms in the adult stage inhabit the nasal fossae and
respiratory tract of vertebrates — chiefly reptiles. They feed on blood
and slimy exudates. The only species known from birds is found in the
air sacs (see Fig. 4 (i) p. 196). The larval form, which is in-
gested in the o^gg stage, invades the viscera of a much wider range of
vertebrates which act as intermediate host, but there are only a few
stray records from birds.

These curious parasites appear like worms — cylindrical, blind and
pale. The body, which is generally a few centimetres in length, is often
divided into rings but these do not correspond to any internal segmenta-
tion. Two pairs of retractile hooks which superficially resemble cats'
claws, and are thought by some to be vestigial appendages, are placed
on either side of the mouth. Respiration is cutaneous. The sexes are
separate. The females are larger than the males and may have over a
million eggs developing simultaneously in their overies.

As we have said, the cheif hosts of tongue- worms are reptiles, which
include some of the largest forms, such as the boa-constrictors, pythons
and crocodiles. Related species from certain genera parasitising
crocodiles and various large snakes, are found in widely separated

MITES 233

parts of the globe, with large areas in between where they are altogether
absent. These two facts suggest that the Pentastomida is a group of
great antiquity, a supposition which is supported by the morphology
of the tongue-worms themselves. The single species which in its adult
stage parasitises birds, Reighardia sternae (order Cephalobaenida), is
placed in a genus and family of its own. It has not yet been recorded
from Britain but as three out of the five known hosts are on the British
list it seems highly probable that in due course it will be found here. The
species has been collected from the common tern in Italy, North
America and China, from the ivory gull in Greenland, and the glaucous
gull from Lapland. The bird tongue-worm is therefore widely distri-
buted, but in this case the discontinuity may be more apparent than
real, as collectors of pentastomes are rather rare and widely distributed
themselves. The intermediate host is not known, but a fish of the herring
group seems a reasonable guess. On the other hand nymphal stages
have been found in the veins of the common tern, which suggests that
development could be direct, without the help of an intermediate host.

There is a single record of a larval form found in a bird on the
British list, namely Armillifer armillatus from the honey-buzzard in
Sweden. This species is a parasite of pythons in the adult stage, but like
many of the spiny-headed worms it apparently has the power of en-
capsuling in a variety of hosts if ingested accidentally and has also
been found at this stage in man, leopards and dogs !

The great interest of the tongue- worms lies in the fact that they are so
modified, apparently by their parasitic mode of life, that no agreement
has been reached with regard to their correct place in the animal king-
dom. At one time or another they have been classified with the flat-
worms, and the roundworms — in fact with all the major groups of
parasitic worms. To-day (1946) they are placed with the Arachnida in
the Zoological Record. Chandler (1946), however, considers them to be
a separate and aberrant class of arthropods. Baer (1946) states that the
tongue-worms are now attached to the annelids or segmented worms.
Heymons, who is probably the greatest authority on the group,
cautiously suggests that they occupy a position somewhere between the
arthropods and the annelids. Their life-cycle, which involves an inter-
mediate host, is certainly reminiscent of the parasitic worms. The first
larval stage when it emerges from the tggy on the other hand, has two
pairs of vestigial legs and resembles a mite. Some authors regard these
legs as atrophied appendages of the arthropod pattern, while others

234 FLEAS, FLUKES AND CUCKOOS

argue that they represent degenerate parapodia of the polychaete type.
In many cases when the adult parasite has been modified beyond
recognition and reduced to a paUid worm-hke organism, the larvae
provide the answer and prove they are cirripedes, copepods or molluscs
as the case may be. But in this instance the larvae, like the adults, have
suffered such a profound change that their present structure merely
presents a series of unanswerable conundrums, which have so far kept
the zoologists guessing.

Female tick, Aponomma sp. (x 8)
with parasitic male attached.

CHAPTER 13

MICRO-PARASITES

For who hath despised the day of small things?

Zeghariah 4 : 10

MODERN PLUMBING Stands between us and daily intimacy with tape-
worms and lice, but most of us are still familiar with the effects of
the microscopical parasites, the bacteria, fungi and viruses. Sooner or
later we contract some infectious or contagious illness, a cold in the
head, boils, ringworm or a more serious disease like measles. The un-
lucky ones may develop tuberculosis or catch infantile paralysis.
Birds are also victims of these microscopic and ultra-microscopic
organisms, but unless they initiate diseases which also affect man, either
directly of indirectly, little is known about them. The average indivi-
dual is unaware that sparrows also suffer from colds in the head and
that wood-pigeons and starlings may contract tuberculosis.

Bacteria

Bacteria, which are usually classified as plants, have been described
by Gardner as minute cells, consisting of semi-liquid protoplasm,
surrounded by a flexible protoplasmic membrane. They lack a cell-
nucleus comparable to the structure common to Protozoa or higher
organisms, although evidence has accumulated which suggests that
there is a nuclear apparatus in many respects analogous to those
characteristic of multicellular plants and animals. In form bacteria
may be spherical or spheroid (Coccus), or rod-shaped, either blunt or
tapering {Bacillus, Bacterium), or twisted and shaped like a cork-
screw {Spirillum, Vibrio). All the motile types possess flagella which are
extremely difficult to see even with a high powered microscope. They

235

236 FLEAS, FLUKES AND CUCKOOS

act as locomotor organs and also help to chum up the nutritive medium
in which the organism lives.

Bacteria usually multiply by binary fission. The cell lengthens to
almost twice its normal size, a septum is formed and it then splits trans-
versely into two halves. After division the cells sometimes adhere to one
another, forming aggregations or chains. Some bacteria produce spores,
a process which might be described as transformation rather than re-
production, since no increase in numbers is involved. The spore stage is
probably a resting phase in which the bacterial cell is more resistant to
unfavourable external conditions. Bacillus anthracis, the causative agent
of anthrax, can remain alive on fields in the spore stage for several
years and resist boiling for ten minutes ! The cyst stage in certain para-
sitic Protozoa and worms is somewhat reminiscent of spore formation
in bacteria.

Owing to their minute size it is difficult to describe these organisms
adequately by morphological characters alone and many bacteria
must be distinguished by their biochemical and physiological functions
and the symptoms they produce in the host. Reactions to dyes and the
body fluids of various animals are also of great importance for the pur-
pose of identification. Their classification, Topley points out, is based
largely on chemical structure rather than the gross architecture of the
cell. Most free-living bacteria are saprophytes, but many commensals
and most of the symbiotic and parasitic forms obtain their nourishment
by decomposing or breaking down living cells or body fluids into a
form which they can assimilate and synthesise into protoplasm. The
harmful effects on the host are due to the poisonous substances which
bacteria produce. These give rise to the various symptoms and lesions
which are characteristic of certain diseases. One of the best known
groups attacking both birds and mammals is the genus Mycobacterium
(family Mycobacteriaceae) . They are so-called "acid-fast" bacteria,
that is to say, once stained with carbol-fuchsin they resist decolorisa-
tion by mineral acids. They are slender, immobile, rod-shaped
organisms which reproduce by simple fission and do not form spores.
They are notorious as the causative agent of tuberculosis, although
some species are harmless saprophytes and inhabit odd media, such as
butter, smegma and the moist surface of timothy grass. Different types
of Mycobacterium are responsible for avian and mammalian tuberculosis
but birds and man do not infect one another. Cows, however, seem to
contract both types in addition to one of their own. Various species of

MICRO-PARASITES 237

wild birds suffer from tuberculosis. In the U.S.A. it has been recorded
from sparrow, crows, cow-birds, pheasants, the sparrow-hawk and
barn-owl. In Britain the disease is most frequently met with in gregari-
ous birds such as starlings, rooks, sea-gulls and wood-pigeons. This is
scarcely surprising, since avian tuberculosis is passed from bird to bird
by contact, or by the accidental ingestion of freshly contaminated
faeces or the exudate from the lungs. In the case of barnyard fowl, which
are also liable to contract the illness, old birds are more susceptible than
young birds. The disease is initiated by way of the digestive tract, not
the lungs, and ulcerative lesions can form in the liver, spleen, intestines,
bone marrow, ovaries, lungs, air-sacs and in fact most tissues. There is
no rise in temperature but a characteristic symptom is the gradual
wasting away of the body, associated with extreme exhaustion. Affected
birds may die within a few months or may survive for several
years.

Another well-known group of bacteria which attack both birds and
mammals is the genus Salmonella (family Bacteriaceae), the causative
agent of typhoid and paratyphoid fever in man, and puUorum disease
and fowl typhoid in birds. These bacteria are primarily intestinal
parasites. They are rod-shaped motile organisms with numbers of
flagella distributed indiscriminately over the surface of the cell. All are
Gram negative, that is to say, they do not retain Gram's stain if de-
colorised by ethyl alcohol or acetone.

Birds are particularly susceptible to Salmonella and no less than
forty species have been described from the fowl in the U.S.A. alone. A
few are host-specific, but many attack a wide range of warm-blooded
animals. Pullorum disease {S. pullorum) has been recorded from several
wild birds including the bullfinch, chaffinch, goldfinch and certain
pigeons. Sparrows, quail, pheasants and bitterns are also susceptible
to experimental infection. This is by far the most important disease of
birds which is transmitted via the tgg. On poultry farms large numbers
of chicks may be infected by contact with contaminated excreta or the
down in incubators, or by contaminated food or water in brooders.
Nevertheless the chief vehicle of infection is certainly the ^gg. In
virulent epidemics the death rate of affected chicks may reach 90 per
cent, or more and pullorum disease has been the cause of huge losses to
the poultry industry. Various other bacteria of the paratyphoid group
have been isolated from wild birds ranging from teal to siskins. Duck
eggs are a recognised source of Salmonella food poisoning in man.

238 FLEAS, FLUKES AND CUCKOOS

The spirochaetes are classified by some zoologists as Protozoa and
by others as bacteria. The electron microscope has shown recently that
at least some spirochaetes possess long filamentous processes. Therefore
the chief feature which was supposed to distinguish them from bacteria
— motility without flagella — seems to have been disposed of. Spiro-
chaetes are active colourless thread-like organisms which can move with
equal ease either backwards or forwards. There is a central filament or
axis around which the body is wound like a spiral staircase round the
newel. The number of spirals varies but is constant for each species.
Spirochaetes reproduce by transverse fission and there is apparently no
sexual process. The best known and most notorious genus is Treponema
which includes the causative agents of syphilis, yaws and relapsing fever.
One species, T. anserinum, parasitises birds and is the cause of relapsing
fever in geese and other farmyard fowl on the Continent. It has not
been recorded from wild birds in Britain, but it is known to infect species
such as the little owl, snipe, sparrow and crow which are on the British
list. Syphilis is spread from one individual to another by contact of
infected surfaces, but relapsing fever of both man and birds is spread by
blood-sucking arthropods. The chief carriers of avian spirochaetes —
of which there may be several distinct species — are ticks of the genus
Argas, but red mites [Dermanyssus gallinae) can also act as vectors.
The spirochaetes are taken up during a blood meal and in the case
of the tick invade the various tissues of the body including the salivary
glands. They also enter the eggs, perhaps as many as thirty to one
Ggg^ and the disease is thus inherited by succeeding generations of
ticks.

Not unnaturally the bacteria which infect birds have been studied
chiefly in poultry. When a particular disease is recognised in chickens
and ducks, particularly if it is the cause of financial losses, it is worked on
fairly intensively and as a result it is often subsequently tracked down in
wild birds. This has been the case with so-called fowl cholera* {Past-

*It is worth drawing attention to the perverse popular names given to the diseases
of pouhry, which might well have been designed especially to confuse the ordinary
parasitologist. Thus the term " fowl cholera" is applied to a disease allied to the
plague or pest, and not even distantly related to cholera of man. Therefore the
true cholera which attacks birds has to be called a "vibrio infection." The term
"fowl pest" is reserved for a disease caused by a virus, which has nothing whatsoever
in common with Pasteurella pestis, the causative agent of plague in man. The well
known and relatively innocuous disease of children known as chicken pox, has on
the other hand, nothing to do with chickens, nor does it attack birds, and it is not
a true pox.

MICRO-PARASITES 239

eurella aviseptica), anthrax [Bacillus anthracis), vibrio infection {Vibrio
metchnikovi) , infectious coryza [Haemophilus gallinarum) and various otlier
diseases caused by the Streptococcus and Staphylococcus type of bacteria,
apart from those ah'eady mentioned. Nevertheless the bacterial dis-
eases of wild birds, particularly in Britain, are virtually unknown.

The organisms described above are all parasites with a marked
pathological effect on the host. There are, however, numerous bacteria
which constitute the normal flora of an animal's body. Some of these
are harmless commensals, others are parasites which have no noticeable
effect except in certain special circumstances when they become
dangerous, and some are definitely beneficial to the host and are thus
more correctly labelled symbionts. There is considerable evidence, for
example, that certain bacteria in the intestines of mammals and birds
synthesise proteins, vitamins and possibly essential amino-acids which
are then used by the host. Some of the invertebrate parasites of birds
apparently depend on the presence of the bacteria associated with the
alimentary canal, for they cannot survive without them. It is always
more difficult to study the beneficial rather than the harmful bacteria,
for the effects of the former are so much less dramatic. In a few cases,
such as the deep sea fish with luminous organs, the relationship is fairly
obvious. The fish possess definite hollow structures, generally situated
on some part of the head, supplied with specialised secretory glands.
The bacteria are present in the water and filter into these special
organs from outside. Once they have gained access they find them-
selves in the presence of a perfect nutrient medium secreted by the
glands in which they luxuriate and multiply rapidly. The highly phos-
phorescent areas which result from these dense aggregations of luminous
bacteria serve the fish as recognition marks, warning signals, or lures to
attract their prey. Very few symbiotic relationships between bacteria
and vertebrates present such a clear cut picture as this, but it is never-
theless highly probable that they do in fact exist between birds and the
microscopical organisms which live in their bodies. This case must not
be confused with the occasional records of luminous bacteria on the
plumage of owls which cause the birds to glow faintly and have given
rise to many terrifying ghost stories. This luminescence is due to the
accidental presence of saprophytic forms which are commonly found
growing on dead meat and fish. The owls acquire them temporarily
from the carcase on which they have been feeding.

240 FLEAS, FLUKES AND CUCKOOS

The Viruses

The viruses are a group of organisms which are nearly all too small
for the eye to perceive even with the aid of a microscope, although they
can sometimes be photographed with the aid of the electron microscope.
Their presence is revealed only when they stimulate some noticeable
reaction in the host. They have never been cultivated outside the living
cell, and the exact nature of a virus is a matter for speculation. They
may be minute micro-organisms somewhat resembling very small
bacteria, progressively degraded by a parasitic form of life which they
have pushed to the utmost limits of specialisation. On the other hand
there is another theory supported by some powerful evidence, which
suggests that viruses are not living organisms at all but chemical sub-
stances— huge nuclear proteins which multiply by so-called auto-
catalysis. Like bacteria and parasitic Protozoa the viruses can reach
their hosts by contact between infected individuals or contaminated
materials including food and water, or by insect carriers; some are air-
borne and others infect their hosts by unknown means.

At least one virus disease, psittacosis, sometimes called ornithosis,
apparently possesses a certain news value. Consequently when a keeper
in the parrot house at the zoo contracts it or an old lady with budgeri-
gars dies of the infection, the British pubHc learn of the occurrence along
with the latest murder story and the football results. The causative
agent is a virus which invades and destroys the reticulo-endothelial
cells, giving rise to clinical symptoms resembhng influenza but often
compUcated by pneumonia. It is rather larger than the ordinary
filterable viruses and falls mid-way between them and the Rickettsia-
like bacteria. Parrots are on the whole more susceptible than other
birds, but pigeons, finches, gulls, ducks, pheasants and fulmars also
suffer from the disease. In the years 1933 to 1937, there were autumn
epidemics of pneumonia among the human inhabitants of the Faeroe
Islands, the cause of which was traced by Rasmussen to a wide-
spread infection among juvenile fulmars which were used by the
islanders to supplement their ordinary diet. Nearly six times as many
women as men were infected and it was assumed that they inhaled the
virus along with a fine dust which is hberated when birds are plucked.
During the war it was discovered that carrier pigeons in Britain were
not infrequently infected with psittacosis, but there were no cHnical
symptoms and it was a type which did not apparently attack man. It

MICRO-PARASITES 24I

is probable that wild birds in Britain are also subject to the disease.

In 1948, Dane recorded a severe epidemic among the manx shear-
waters on Skomer Isle. Hundreds of juvenile birds died in outbreaks
which occurred in two consecutive breeding seasons. The causative
agent was a virus and the visible symptoms included blisters on the
webs of the feet, inflammation of the eyes which led to blindness, and
extreme exhaustion sometimes accompanied by unnatural extension of
the legs. Some similar symptoms had been observed in three juvenile
herring-gulls which died on nearby Skokholm Isle, and it seems probable
that the disease is not confined to shearwaters. Ducks have been in-
fected experimentally.

A world-wide virus disease of chickens is popularly known as fowl-pox.
The organism concerned is related to the virus of small-pox and cow-
pox. In the days before vaccination, chickens which contracted the
disease were regarded with grave apprehension, as they were considered
a possible source of human epidemics, but it is now known that fowl-
pox is not transmissible to man. Moreover several different types of pox
are known which attack birds — fowl-pox, pigeon-pox and canary-pox.
Pigeons are resistant to fowl-pox, but chickens contract a very mild
form of the disease if exposed to pigeon-pox, which then renders them
immune to the deadly form of their own variety. In the same way an
attack of cow-pox immunises man against small-pox. A pigeon-pox
vaccine is now used widely to protect chickens against the disease.
Various mosquitoes are proved carriers of fowl-pox. They mechanically
transmit the virus from one bird to another. The house-gnat remains
infective for 58 days after feeding on a diseased bird. It is remarkable
that some strain of the virus has not become acclimatised to man, since
it must continually be introduced into his body by this insect. The same
applies to the avian Plasmodium, Canary-pox is also a disease of wild
sparrows in the United States and several outbreaks among them have
been studied. Quail, grouse, pheasants, partridges and pigeons are also
subject to natural infections of avian pox of one type or another. The
disease almost certainly occurs in wild birds in Britain.

There are of course other viruses recorded from birds, apart from
the three selected above; for example, the causative agents of Rous
sarcoma, fowl paralysis, fowl leukaemia and fowl pest. In Italy a
previously unknown virus has been recorded from wild thrushes and
another from owls in the United States. No doubt many others await
discovery and investigation in wild birds in Britain.

242 FLEAS, FLUKES AND CUCKOOS

Fungi

Fungi are plants without chlorophyll which live as saprophytes,
parasites, commensals or symbionts. All the species attacking birds and
mammals are facultative parasites which pass from a saprophytic mode
of life because conditions happen to favour the change. Fungi
attacking other plants are often obligatory parasites and strictly host
specific.

The parasitic fungi of birds are microscopic organisms and the
reader will be disappointed if he expects to see a robin with a large
mushroom sprouting under its wings or from between its toes. The
host's reactions to viruses and bacteria are visible to the naked eye and
one can see pockmarks and boils. Similarly, fungi are responsible for
obvious lesions, such as the red patches of ringworm, but the causative
organism has to be sought and examined with the aid of a microscope.
The general appearance and colour of colonies of fungi grown in the
laboratory are however of great importance for the purpose of identifica-
tion.

A typical parasitic fungus consists of filamentous branching threads
or hyphae, with a tough chitinous outer covering, collectively forming a
mycelium, which ramify through the tissues of the host. These fila-
ments absorb the decaying substances or solutions in which they are
immersed and can also secrete various enzymes which assist them in the
process of decomposing organic matter. Fungi reproduce either by a
sexual or asexual process. They give rise to spores which are extremely
long lived or resistant and can germinate after a resting period of 20
years or more.

In many respects fungi resemble bacteria. In some forms the my-
celium breaks down and forms chains of cells, or fragments into separate
cells, and in these stages it is virtually impossible to distinguish them
from bacteria. Conversely in some classifications, certain bacteria are
placed among the fungi and the mycelium is described as "rudimentary
or absent."

Diseases which result from attacks by fungus are known collectively
as the mycoses. A great variety parasitises man and in his Precis de
Parasitologie Brumpt considers them sufficiently important to assign
them 429 pages out of a total of 2,064. Some of these species also
attack birds. Favus, which is a chronic mycosis of the skin, is produced
by various members of the genus Achorion. Thrush, a mycosis of the

S. C. Porter

a. Common house-martin fiea, Cerato-
phyllus hirundinis, male at rest ( x i6)

S. C. Porter
b. Common house-martin flea, C. hirun-
dinis, about to feed ( x i6)

Arthur L. E. Barron
c. Terminal portion of leg of shearwater flea, Ornithopsylla laetitiae ( x 205)
Plate XXXIII

Eric Hosking

a. Cormorants breeding in a colony : colonial nesting favours a high rate of infection with
bacteria as well as fleas and other ectoparasites

Money Salmon {by flashlight)
b. Shearwater at entrance to its burrow: host of the most interesting British bird flea,
Ornithopsylla laetitiae, only known from the British Isles. This bird is attacked by a latal

virus disease
Plate XXXIV

MICRO-PARASITES 243

mouth and intestinal tract, is due to infection with the genera Monilia
and Oidium. Perhaps the best known fungus parasitising birds is
Aspergillus fumigatus (see tail-piece Chapter i, p. lo), which is localised in
the respiratory tract. The spores of this plant are widely distributed in
nature and the birds inhale them with dust or pick them up with
mouldy food or water. They form colonies in the lungs and air passages
and some birds are highly susceptible to the bacteria-like toxins they
produce. Several allied species are known and sometimes multiple in-
fections occur when Penicillium and Mucor moulds are found in associa-
tion with Aspergillus. We have frequently observed mycosis in wild
wood-pigeons from all parts of Britain and Dane records A. fumigatus
in the air sacs of the manx shearwater.

As we have seen in the preceding chapters, fungi are also most useful
to birds since they are hyper-parasites of many species of arthropods
and helminths which parasitise avian hosts. One of the best known
genera is Empusa (Entomophthoraceae) of which various species cause
a fatal disease in mosquitoes (including the house-gnat) and other
Diptera such as blow-flies, house-flies, and midges, and also in mites.
Large numbers attack roundworms at all stages of their development.
Some extremely interesting fungi, such as the genera Dactylaria and
Dactyella (Hyphomycetales), capture certain parasitic nematodes alive
during their free-living stages. They are snared by means of loop-
shaped portions of the mycelium, each of which operates on the Hues of a
sphygmomanometer. Contact with the prey causes the loops to swell
suddenly and constrict round the worm which is held fast and ulti-
mately consumed.

There is a curious and obscure group of parasites, the Sarcosporidia,
members of which are located in the striated muscles of mammals and
birds. At one time they were classified as Protozoa but are now con-
sidered to be fungi. Surface feeding ducks are the most heavily infected
group, but they have been recorded from 28 species of birds from
eight different orders. The larger forms of the parasite can be seen as
httle white streaks in the striated muscles which give the fibres a
"wormy" appearance. When removed from the tissues each resembles a
minute colourless spindle. The body is divided into chambers, which,
in fully developed specimens, are filled with sickle-shaped spores. The
life-cycle of Sarcocystis is not properly understood, although there is
some evidence that infection can occur after ingesting urine and faeces
from animals with the disease. On the Continent avian sarcosporidiosis

FFC— R

244 FLEAS, FLUKES AND CUCKOOS

has been recorded from several common birds on the British list
such as the blackbird and sparrow, and there seems little reason to
doubt that it will eventually be found in this country.

The relationship which exists between parasitic fungi and bacteria is
one of the greatest interest. In many cases these two types of organism
compete with one another in the same environment. Often the presence
of bacteria in a culture of fungi arrests its development, but in other
cases they seem to exert a beneficial influence. Certain Staphylococci,
for example, stimulate the growth of Achorion^ and in the presence of
bacteria (but not in pure cultures) Aspergillus produces spore-bearing
perithecia. On the other hand it is now known that extracts of
certain fungi have a powerful antibiotic or lethal effect on various
bacteria. In 19 13 Vaudremer showed that a filtered extract o^ Asper-
gillus fumigatus inhibited the growth of tubercle baciUi. In recent years
penicillin has been extracted from various species of Penicillium
(especially P. notatum) and has proved the most powerful antibiotic ever
known. An extract from another fungus, Streptomyces griseus, now known
as streptomycin, also exerts a powerful lethal effect on certain bacteria,
among them species such as the tubercle bacillus, which is not affected
by penicillin. The secretions of fungi have consequently provided one
of the great discoveries of the age.

CHAPTER 14

THE FAUNA OF BIRDS' NESTS

. . . this bird
Hath made his pendant bed and procreant cradle :

Shakespeare

Birds' nests, as Waterston remarked with masterly understatement,
must make lively nurseries. It is the really snug nests, built
under eaves or placed in holes, like those of martins and jackdaws,
which provide the offspring with an early insight into the grim realities
of life. Even migration must seem a picnic in comparison with the tor-
tures of nestling days. Young wood-pigeons, which squat precariously
on a flimsy raft high up in the branches, have a very easy time in com-
parison, and could well look back with nostalgic regret on the period
of pigeons' milk passed among the swaying tree tops.

The inhabitants of birds' nests, other than the rightful owners, are
chiefly arthropods. Insects and mites predominate, although ticks,
pseudo-scorpions, spiders and an occasional centipede, wood-louse, or
free-living nematode may also be present. In Finland, Nordberg
studied the fauna of 56 species of birds' nests, from which he recorded
no less than 529 different kinds of arthropods. Beetles accounted for
118 species and mites another 228. The rest consisted of bugs, flies,
fleas, ticks, feather lice, moths, springtails, earwigs, book-lice and a few
parasitic Hymenoptera and spiders. A number of permanent obligate
ecto-parasites, such as the feather lice, occasionally wander off the host,
possibly in the process of transferring themselves to the nestlings, and
are found in the nest, but they are not true nidicoles, as their proper
habitat is the host's body. In addition, about a third of the species
found in birds' nests are purely casual or accidental visitors. Another
large category includes species which frequent various micro-habitats
that afford conditions similar to those of nests. Thus many beetles which

245

246 FLEAS, FLUKES AND CUCKOOS

are found in nests in holes are equally numerous in holes without nests.
There are also many common plant-eating mites and insects which are
passively introduced along with moss and lichen and other vegetable
nesting material. These flourish in a wide range of bird habitations,
and, ill cases such as the mite, Oribata geniculatus, can become dominant
species, but they are in no way peculiar to this type of habitat. Despite
the large proportion of wanderers, accidental visitors, occasional and
casual residents, and constant if independent inhabitants, there remains
quite a high proportion — say between 20 and 25 per cent. — of the
species present, which at one stage or another of their life-cycle are
obligate nidicoles and dependent on nests. Of these a few are host-
specific, and are found only in the nests of one species, or of a group of
related species of birds, but many are catholic in their tastes.

Various factors influence and determine the fauna of birds' nests,
and our knowledge concerning them is ridiculously small, but one or
two generalisations can be made with confidence. Nests which are
built in holes, and which are returned to and re-occupied year after
year, contain on an average a larger number of individual nidicoles
and a greater variety of species than other nests. In this respect the host
itself seems to be less important. Thus the wood-pigeon has the smallest
nest fauna of any British bird so far examined, both as regards numbers
and variety, and the closely related stock-dove, which generally nests
in holes, has the largest. Needless to say there are many exceptions.
The crow family as a rule have revoltingly verminous nests, and the
carrion-crow with about 80 species recorded can boast a richer fauna
than most hole dwellers. The type of nest, whether it is domed or flat,
or just a scrape, massive or flimsy, constructed of mud or moss, stick or
stones, sea-weed or sand, naturally influences the nest fauna. The site
chosen, the age of the nest, whether it has contained young, its distance
from the ground, the proximity to water or human habitations or other
birds' nests is also important. The habits of the host, particularly its
choice of food, which to a great extent determines the nature of the
debris within the nest, have a considerable bearing on the species
of arthropods found there. Thus a beetle, Trox scaler, which chiefly
feeds on old bones and hides, is characteristic of owls' nests and
one would not look for it under a sitting firecrest or blackcap.

The population of a bird's nest is not, of course, stable. The various
nidicoles have different requirements of food, temperature, humidity
or light; and this will influence which species occur in specific nests, in

THE FAUNA OF BIRDS* NESTS 247

which part of the structure and at what period of their history. Thus
within the nest itself there may be different levels at which various
species are more abundant than at others. For example, in a great tit's
nest, out of a total of 3,469 arthropod inhabitants, 490 were found in
the lining, 2,277 in the middle layers and 702 in the outer structure.
In a flycatcher's nest the position was reversed and out of a total of
1,568 specimens no less than 840 — over half — were found in the lining,
and the smallest numbers were present in the middle layer, where, in
the tit's nest, they reached a maximum. An observer once saw fly
larvae — up to that moment completely hidden — seethe to the surface
of the lining when droppings fell, and eagerly devour them. The nest is
occupied however, for only a very brief period and most populations —
especially if the larvae and adults of each group are counted together —
reach a maximum density during two or three days when the young are
about to leave or have just flown. Quite a large assortment of arthro-
pods overwinter in immature or adult stages in the nest.

The habitations of the Hirundinidae (martins and swallows) probably
harbour the most interesting nidicoles of any group of British birds,
although several others, such as the jackdaw, starling and stock-dove
have a larger assortment. The crows as a family, have a richer though
less distinctive nest fauna.

A conspicuous inhabitant of house-martins' and occasionally other
birds' nests is the swallow bug {Oeciacus hiriindinis, Plate XXXVIb).
We have already remarked (p. 16) that martins and men probably
shared cave dwellings in prehistoric times and they may both have
acquired this group of parasites in their former habitat. Very few birds
are preyed on by bugs. One of their essential requirements is a perma-
nent dwelling house, for during the day they hide in cracks and crevices
— in which they also lay their eggs — and only creep out at night for a
blood meal. There is one other bird bug in Britain, Cimex columbarius^
which is a parasite of the domestic pigeon. In all probability it is a
sub-species of the human bed-bug (C lectularius^ see Plate XXXVIa)
which has passed accidentally on to pigeons and chickens since their
domestication by man, and has now become morphologically distinct.
Fertile hybrids can be obtained by crossing the two forms. The bugs
which infest wild birds can only survive if the host is the type which
returns to its old nest. Moreover the nest itself must remain fairly dry
during the host's absence. In the United States the barn-swallow [Hirundo
rustica erythrogaster) and purple martin {Progne subis) , and the oven-bird

248 FLEAS, FLUKES AND CUCKOOS

{Furnarius rufus) in South America, harbour related species of bugs.
The majority of other bugs (Hemiptera) are plant suckers, but they are to
a certain extent preadapted to an ecto-parasitic mode of life, as they are
flattened dorso-ventrally and have piercing mouth-parts. Many free
phytophagous bugs show a tendency to winglessness, and in some
species one sex has wings and the other has not (p. 52). Some
of the assassin bugs (Reduviidae) which normally prey on other
insects, have become voracious blood suckers and are often found in
birds' nests in America. Only one family, the species of which live
on bats, have evolved into true permanent obligate ecto-parasites.

An Anthocorid bug, Lyctocoris campestris, is a cosmopolitan species
also found in house-martins' nests in Britain. It is a predator which
sucks mites and the pupae of fleas but since it has also been known to
feed on human blood its activities in the nest are not beyond suspicion.
It probably competes with the pseudoscorpions — arthropods looking
like miniature crayfish — which hunt and eat mites. One in particular,
Chelifer cancroides, is a constant species in the nests of swallows and
martins. It is a great hitch-hiker (see p. 18) and is carried to new
feeding grounds attached to various insects, especially flies, which it
clasps firmly with its huge pincer-like claws.

Swallows, house-martins, and also house-sparrows and to a lesser
degree flycatchers, which in Britain nest so frequently on man-made
buildings, often harbour certain nidicoles for which they and their
human neighbours can blame one another. Thus five indigenous
species of dermestid beetles are found in their nests and except for
Dermestes murinus, which is common in the habitations of various birds
of prey, these are only rarely recorded from other wild birds' nests in
Britain. Both larva and adult of D. lardarius and D. murinus feed on
stored products such as dried and smoked fish and meat, cheese, dried
milk, bones, dried insects and so forth. To a certain extent D. lardarius
is predacious and if present in large numbers occasionally attacks and
kills nestling birds. It has been known to bore into the wing bones of
young pigeons and eat them alive. In nests these beetles also feed on
dried insect remains, which seem to be a favourite food, for in nature
dermestids are also found commonly in wasps' and bees' nests and
caterpillar webs. Attagenus pellio, another dermestid found in the same
birds' nests as the previous species, feeds on nectar as an adult,
but the larva favours a diet of feathers, dead insects, furs, skins,
woollen carpets, grain and cereal products. These beetles are scarcely

THE FAUNA OF BIRDS* NESTS 249

welcome guests, but there are several groups of Coleoptera which prey
on the parasites of the birds, especially fleas and their larvae, and can
therefore be regarded as symbiotic partners. Foremost of these are rove
beetles (Staphylinidae) and histerid beetles (Histeridae). The former
family is extremely interesting (see p. 50), since many species have
become adapted to life in nests — of colonial and gregarious insects as
well as of mammals and birds — all over the world. In this country the
genus Microglotta is the most noteworthy. The insects feed on fleas and
their larvae. It seems possible that the species in birds' nests such as
M. nidicola and M. pulla can only breed at a temperature between 36°
and 40°G. — in other words when the parent birds are brooding.
Although these beetles often remain in deserted nests and wander into
ants' nests, they apparently do not breed there and Heim de Balzac
suggests that high temperatures are necessary to bring about the
maturation of the gonads. In Britain M. nidicola is confined to nests of
the sand-martin and is found in about 70 per cent, of their burrows —
sometimes more than fifty specimens in one nest. Other species recorded
from this country are M. picipennis, apparently confined to buzzards'
nests in Britain, but found in those of a variety of birds of prey on the
continent, and M. gentilis, which favours owls' nests.

A wide range of hosts seems suitable for M. pulla, which has been
recorded from the habitations of many birds, but shows a predi-
lection for those of tits. There are of course various other rove beetles
associated with birds' nests, of which perhaps Atheta nidicola and
A. nigricornis are the most characteristic. Although recorded from
martins' they are more commonly met with in other nests. Spittle has
found both in the nests of the heron and carrion-crow along with a
third species, A. trinotata, which unlike the previous pair is not pre-
dacious but parasitic upon anthomyid fly larvae and pupae. One
species, A. oloriphyla, was first found in 1933 in a swan's nest and has not
been recorded since. Other typical genera are Philonthus (P. fuscus
seems confined to birds' nests) and Aleochara. Of the Histeridae the
genus Gnathoncus is a voracious eater of fleas in all stages of development.
Curiously enough it is absent from the martins' nests, which have the
highest flea population known (see p. 109). It is possible that it has a
liking for certain species, e.g. the hen flea (C gallinae)^ but not for others.
A wide variety of nests harbour G. punctulatus, (see tail-piece Chapter 7)
and in Finland it is a constant and sometimes dominant species in the
nests of the house-sparrow, great tit and similar birds which are usually

250 FLEAS, FLUKES AND CUCKOOS

infested with the hen flea. Two other species, G. nidicola and G.
buyssoniy are recorded from owls' and hawks' nests in Britain. Some-
times the adults develop a perverted taste and chew the feet of sitting
birds. However Gnathoncus is generally modestly represented compared
with its prey. A flycatcher's nest harboured 170 specimens, a great
tit's 58, a chaffinch's 34, and 14 were taken by Spittle from an owl's
nest. Three other British histerids found in birds' nests are Dendrophylus
punctatuSy D. pygmaeus, and Hister merdarius. In addition to the predatory
beetles there are numbers which perform a useful function by scaveng-
ing in the nests of their hosts. We have already mentioned the beetles
Trox scaber and T. scabulosa which are very common in nests of birds of
prey where they feed on bones and hides. Over 100 specimens have been
recorded from one nest. Beetles of the family Lathridiidae, such as
Enicmus minutus, which feed on fungi both as adults and larvae, are
frequent occupants of a wide range of birds' nests, and act as scavengers.
About 40 species of beetles have been recorded from hirundinid nests
in northern Europe, but the jackdaw can probably boast the greatest
attraction for Coleoptera. Over 50 species have been recorded from its
nest alone. Nordberg, by a somewhat abstruse calculation, found there
were 280 beetles per cubic decimetre of jackdaw nesting material !
Few birds, however, harbour a host-specific beetle. Probably the only
avian host in Britain thus distinguished is the sand-martin.

Even more peculiar is the fact that the sand-martin is parasitised by
a host-specific tick, Ixodes canisuga. As we have seen (p. 229) ticks are
rarely host-specific — and in this respect, as well as many others, the
sand-martin is unique among British passerine birds. The mite fauna
of birds' nests is extensive, consisting of species which are parasites of the
host or other nidicoles, or are scavengers and plant eaters. The martins
have several species which are peculiar to them.

Certain clothes moths are also found in birds' nests ; Tinea pellionella
is a common species in martins' and sparrows' nests. The larva feeds on
the lining but it also chews up expensive materials such as carpets, fur
coats and cushions in the houses on which the birds have built their
nests. A predator of the larva, the window fly (Scenopinus fenestralis) has
occasionally been recorded from nests. Another related moth, T, lapella
(see tail-piece of Chapter 2, p. 19), is an obligate commensal of certain
passerine birds like the hedge-sparrow and thrush. The larva also feeds
on feathers, and although there are presumably many other sources of
keratin available this moth has up till now been found only in nests, and

THE FAUNA OF BIRDS NESTS 25I

is far more closely linked with this habitat than the previous species.
The commonest moth in swallows' and martins' nests in England is
Hofmannophila pseudospretella and it has also been bred by Basden from
nests of the barn-owl, wren and starling. The larvae are scavengers and
will feed on faeces, dead nestlings and even addled eggs. Two other
moths, Monopis rusticella and M. ferruginella, are also commonly associ-
ated with nests of many birds in this country. There are, however, in
Britain, no true symbiotic moths comparable with the species usually
present in the nest of the Australian golden-shouldered parrakeet [Psepho-
tus chrysopterygius) . The larva of this moth lives unobtrusively in the
bottom of the nest, and, hke a well-trained nurse-maid, not only tidies
up the nursery, but with meticulous care cleans the droppings off the
nether limbs of the nestlings.

Chief among the scavengers are the fly larvae. As we have seen in
Chapter 12, some of these have become true ecto-parasites on the
nesthngs and some facultative parasites, but there remains a fair number,
such as species of Fannia, Anthomyia, Hydrotaea and Phaonia, which, as a
rule, feed on refuse in the nest, although at times they may be semi-
predacious. A few species also parasitise other dipterous larvae.
Occasionally the magnificent metallic corpse-feeder Cynomyia mortuorum
is found in nests, and probably the larvae are not above suspicion
as facultative parasites. True parasites of nestlings are the larvae
Protocalliphora and Neottiophilum^ which are dealt with in Chapter
II (p. 221). Camus and Meoneura are thought to be ectopara-
sitic as adults, but their larvae probably live as scavengers in the
nest. There are also some groups of flies, Phoridae, Helomyzidae and
others, which occur quite frequently and are vegetable refuse eaters, but
are also found in carrion, dung and fungi. There are also a few
Hymenoptera which parasitise the larvae of fleas, flies and moths, and
are no doubt extremely useful to the birds.

Generally each bird or group of birds has a characteristic nidicolous
fauna, in which certain species are found more frequently than others
or in larger numbers. In martins' nests in Britain, fleas are the
dominant and most important group (see p. 80). They are present
in over 80 per cent., and their numbers are greater and their species
more varied in these than in other birds' nests. Flies are the next
most important group, followed by moths. Here, however, there is
a divergence between the fauna of the ground nesting sand-martin
and the house-martin and swallow. Moths are an important group in

252 FLEAS, FLUKES AND CUCKOOS

the latter's nests, but uncommon in the former's, where mites take their
place as a dominant group.

It will have become evident from this brief account, mainly of the
fauna of martins' and swallows' nests, that the bird-lovers who carefully
preserve their habitations from one year to another also unintentionally
preserve the louse-flies, fleas, mites and bugs over-wintering as larvae
and pupae or hibernating in the nest, which are directly responsible for
bringing hours of pain, miser\% disease or even death to the nestlings in
the following spring. Under these circumstances it seems astonishing
that birds returning from their winter quarters, especially those which
feed on insects, do not rid their own nests of nidicoles before reoccupying
them. They are, however, creatures of habit and inflexible instincts.
Hedge-sparrows and other species (see p. 261) will let their own young
die of star\'ation if they are shifted from the inside to the edge of their
nests. In such a position they are not recognised as nestlings and are
not fed. It is possible that birds do not associate food-hunting with the
nest, but in its presence respond to a strong instinct to be unobtrusive
and quiet, and to disturb it as little as possible. They may not, there-
fore, recognise the nidicoles as food. Furthermore, these arthropods
may be highly unpalatable. The smell of bed-bugs does not suggest that
they would form an attractive breakfast. On the other hand, recent
visual obser\'ations made on rooks during sexual display and courtship
in the rookerv^ in winter show that they obtain a considerable amount of
food from their nests. The photograph on Plate XXXMI of a whitethroat
is a source of speculation. "WTiat, in fact, is it doing? Removing faeces
from the nest or routing out nidicoles? Possibly birds do destroy num-
bers of these arthropods. In any case it is an aspect of bird behaviour
about which little, if anything, is known and it should prove yet
another interesting and fruitful source of study.

CHAPTER 15

SKUAS

Sailing on obscene wings athwart the noon . . .

Samuel Taylor Coleridge

INCIPIENT or casual clepto-parasitism among birds can be seen by
anyone who visits the Serpentine on a cold winter afternoon and
watches the gulls and diving ducks.

Children often throw large chunks of bread into the water which are
hastily seized by the tufted ducks. While they are attempting to swallow
these unwieldy pieces the gulls dash at them and try to harry them or
startle them into dropping the bread into the w^ater. The ducks
frequently dive to escape from the gulls, which hover over the water and
pounce again immediately after the ducks surface. Quite often, owing
to their wonderful powers of flight, their dash and persistence, the gulls
manage to appropriate the bread for themselves. This behaviour is the
result of the unnatural conditions prevailing on the Serpentine, where
all the birds are crowded together round an artificial source of food,
but it proves how, in certain circumstances, species which are not
normally clepto-parasites can modify their behaviour in that direction.
A more curious episode of this type was once observed in the farmyard.
A cockerel, wdth great dash and daring, rushed up to a cat and seized
and swallowed the mouse with which it was playing.

The only real British bird clepto-parasites are the skuas, but it is
perhaps worth mentioning one or two foreign species which have
developed a slightly different form of the same habit.

The American wigeon {Anas americana) — a rare vagrant in Britain —
associates with coots and robs them of the weeds which they obtain by
diving under water but subsequently bring to the surface to eat. This
is probably an extension of a commensal relationship similar to that
which exists between our wigeon and brent geese.

253

254 FLEAS, FLUKES AND CUCKOOS

A stranger form of clepto-parasitism is practised by certain tropical
thrushes (Turdidae), particularly of the genus Aleihe, which are often
referred to as "ant-birds." They have developed the habit of following
parties of driver ants and, in addition to catching insects which may
be flushed by foraging columns, they actually rob the ants of the prey
which they are carrying. In the Belgian Congo, Chapin once observed
small parties of thrushes and bulbuls (Pycnonotidae) waiting alongside
a forest road and robbing the ants when they were forced to expose
themselves to view in the open while crossing from one side of the road
to the other. The frigate-birds (Fregatidae), of which there are five
species, are related to our gannets and cormorants. They range over
the tropical seas, sailing around throughout the day on motionless
wings, sometimes rising to great heights until they are mere specks in
the sky. At sundown they return to the shore and roost communally in
convenient trees. They never settle on the water and this particular
aversion may well be one of the factors contributing to the development
of the clepto-parasitic habit. If there are shoals of pelagic fish within
sight they swoop down and take their choice almost without ruffling
the surface of the sea. If such prey is scarce they pursue other birds and
force them to disgorge their food, either from their beaks or their crops.

The skuas are brown, gull-like birds, which range across the northern
and southern oceans at all distances from the shore, spending most of
their lives at sea, and unlike the frigate birds do not return to land to
roost. They, also, obtain a large proportion of their food by robbing
other birds. There are four native species, but of these only the great
skua and the arctic skua breed in Britain. The long-tailed skua and
pomatorhine skua are passage migrants and seasonal visitors.

The great skua is essentially a maritime bird and is rarely seen in-
land. It is a little larger than a herring-gull, dark brown in colour, with
a white patch at the base of the primary wing feathers. In the spring it
resorts to elevated moorlands and rough hilly pastures near the sea,
where it breeds in colonies. The nest is little more than a scrape lined
with heather and moss. As a rule it lays two eggs, which are usually
olive-grey or reddish-brown with dark brown spots and blotches. Both
sexes incubate the eggs and when the young hatch the male provides
their food while the female broods them.

Most of this food is obtained by piracy. The great skua pursues a
number of different species of sea birds, chiefly gulls — even those which
are larger than itself, such as the greater black-backed gull. It attacks

SKUAS 255

with great dash and agility and, with quick stoops and swerves, worries
and frightens the quarry until it abandons its catch in mid-air or dis-
gorges its last meal. Very often the skua, with a graceful aerial dive,
catches the fish, or whatever the prize may be, before it falls into the sea.
Meinertzhagen noticed that skuas in the Shetlands adopt a special
method of robbing gannets. They seize the tip of the gannet's wing,
causing it to crash into the sea and flounder helplessly in the water.
The skua only lets go when the gannet has disgorged. At other times
the skua seizes the gannet by the tail and tips it up into the water.

The arctic skua, which is the commonest British species, is a smaller
bird and easily distinguished by the two long straight feathers projecting
from its wedge-shaped tail. These are clearly seen on Plate XXXVIIIa
Its upper parts are uniformly brown, but the breast varies considerably
and is sometimes almost white. Its habits are similar to those of the great
skua, although in stormy weather it is more often seen inland. The
arctic skua also obtains its food principally by piracy. It concentrates
more on the smaller gulls, such as the kittiwakes and terns, but it also
pursues puffins and guillemots. When the skua has selected a victim
it follows it with great persistence, turning and twisting with amazing
agility and chasing it relentlessly until the food is dropped. It then
catches it with a single stoop and swallows it in mid-air. Despite their
piratical habits the skuas are all capable of capturing their own prey.
Apart from fish and other marine organisms they kill and eat a wide
range of young birds and some adults, devour eggs and carcases and
various insects including beetles and dragon-flies. They also take
small mammals at their breeding haunts, and have even been known to
kill lambs.

CHAPTER l6

THE EUROPEAN CUCKOO

And these are they which ye shall have in abomination
among the fowls . . .

Leviticus 11:13

THERE ARE about 200 different species of cuckoo, but only one breeds
in Britain — the European cuckoo (Plate XXXVIIIb). The ancient
Hebrews were possibly deceived by its hawk-like appearance and, for
this reason, may have prohibited it, along with the nightjars and the owls,
as an article of diet.* Most casual observers to-day who catch sight of a
cuckoo beating along open hedgerows, or gliding out of a thicket or
copse, mistake it for a bird of prey. It must be admitted that in
silhouette, colouring, size and flight it is superficially very like a
sparrow-hawk. Compared with some of its foreign relatives it is a drab
bird. The upper parts and breast are blue-grey and the remaining
under-parts whitish with dark bars. The legs and feet are yellow. In
Asia, India and Africa many cuckoos are brilliantly coloured — bright
metallic green, purple, bronze, golden and pied. Quite a large propor-
tion of the American species — most of which are not parasitic —
are terrestrial birds, which rarely use their wings, but can put on an
amazing turn of speed running across country or through dense
undergrowth.

The song of the male cuckoo is too well known to require descrip-
tion, but in these days of specialisation many naturalists are unaware
that the female of the species does not "cuckoo" at all, but has a soft
bubbling call — rather like a sudden rush of water through a narrow-
necked bottle. Almost everything about the European cuckoo is peculiar,
even its diet. Hairy caterpillars constitute its favourite food — a form of
nourishment which no other bird would touch — and their hairs become
imbedded in the cuckoo's gizzard so that it appears to be lined with

y * According to the Authorised Version.

256

THE EUROPEAN CUCKOO 257

dense fur. This diet is an inherited rather than an acquired taste, which
develops once the cuckoo has left the care of its foster-parents — no
matter what form of food it has previously received from them.

When the cuckoo returns from its winter quarters in Africa, the
female selects a territory for herself, preferably in rather open country.
Sometimes she returns to the same area several years running. In the
case of the European cuckoo the territory is a few acres in extent, but
in some African species such as the small golden cuckoo [Lampromorpha
caprius), which victimises colonial-nesting weavers, it may be restricted
to one tree. She defends this territory against all other female cuckoos
parasitising the same fosterer as herself Although successful invasions
sometimes occur it is unusual to find two female cuckoos in the same
area laying in the nests of the same species of small bird. Individuals
parasitising other hosts are tolerated. Occasionally a young bird which
has failed to establish a territory of her own will roam across country,
laying at random in any available nest she can find.

The male cuckoo also establishes a territory, but in the case of the
British species it rarely coincides with the territory of any particular
female. He favours wooded areas or the edge of small copses rather
than open country. The cuckoo's relations with the opposite sex are
distinctly casual and very promiscuous. Sometimes numerous males
gather when they hear a female's amorous bubbhng and she may
copulate with one, two, or all of them. At other times one particular
male may seek her out persistently and thus give the impression that
they are permanently paired. Again, a male bird may haunt several
adjacent territories, bestowing his favours freely on all the female
owners.

The female cuckoo hunts systematically for the nests of her victims,
which are generally small passerine birds— chiefly those which feed on
insects. Quite often though, the linnet, which is a seed eater, is chosen.
When she locates a pair building she begins a careful and prolonged
vigil, observing the behaviour and movements of the future fosterers
from a point of vantage and sometimes gliding down to examine the
nest at close quarters. The visual stimulus thus received appears to
excite ovulation and the cuckoo's egg reaches maturity and is ready for
laying about five days later, in fact shortly after the fosterers have them-
selves begun to lay.

Most birds deposit their eggs early in the morning, but the cuckoo
does so in the early afternoon, a period at which the parent birds —

258 FLEAS, FLUKES AND CUCKOOS

providing their clutch is incomplete — arc most likely to be absent. She
glides over the selected nest several times and then quickly alights in it
and lays one egg directly into the nest — the entire action occupying
no more than five seconds. Subsequently she destroys one or more of
the fosterer's eggs, either by throwing them out or by crushing and
eating them. Sometimes she carries one a considerable distance in her
beak before disposing of it. When the cuckoo deposits her egg in a small
domed nest with a side entrance it is impossible for her to enter and lay
in the usual manner. The egg is then forcibly projected into the aperture
from the bird's cloaca while she hovers immediately over the nest — a
feat which might excite envy in an Olympic athlete. Some hold the
view that on certain occasions it is first laid on the ground, picked up in
the cuckoo's beak and then dropped into the nest. Whether this some-
times happens is a matter of acute controversy. The majority of eggs (if
not all) which are seen being carried by cuckoos are not their own, but
eggs of the fosterers which they are about to destroy.

If conditions are favourable and there are enough breeding pairs
of the right species of fosterer present, with incomplete or just completed
clutches, the female cuckoo will continue laying eggs at intervals of
about forty-eight hours until between fourteen and twenty have been
deposited. One female parasitising meadow-pipits has been known to
lay twenty-five eggs in one season. There are, however, rarely enough
nests available in a single territory to make such a feat possible, although
the cuckoo is able to keep several under observation simultaneously.
On occasion she will destroy a whole clutch in order that a particular
nest should be in a suitable condition to receive one of her eggs at a
later date. Some species such as the great spotted cuckoo lay several
eggs in the same nest, but the European cuckoo almost always distri-
butes her eggs singly.

It is now a well-estabhshed fact that there are strains or "gentes" of
the European cuckoo which, throughout their Hves, parasitise only one
particular species of small birds. In Britain there are relatively few
regular hosts. The main fosterers used are the meadow-pipit, the robin,
the pied wagtail, the hedge-sparrow, the reed-warbler and the sedge-
warbler. In Germany a favourite host is the red-backed shrike, which is
rarely, if ever, attacked in Britain. In Finland, on the other hand, the
most popular fosterers are the redstart (which is rarely parasitised in
Germany), the wheatear, the whinchat and the pied flycatcher, all of
which lay blue eggs. In Finland 68 per cent, of cuckoos' eggs are blue,

2QI "'^pR.:

Plate XXXV Eric Hosking

Sand-martin at nest burrow : this long and sandy burrow, excavated by the sand-martin for its
nest and to which it returns year after year, harbours an unusually interestmg parasitic and
commensal fauna, of which' certain species are exceptionally abundant and host-specihc

. o

.i2

3
C/3

C/2
O

THE EUROPEAN CUCKOO 259

whereas in England they are almost all of the spotted type. The number
of eggs laid by individual cuckoos depends to a certain extent on the
species of host favoured. Thus, in Germany "red-backed shrike"
cuckoos lay fewer eggs than "robin" cuckoos, for the breeding season of
the former host is much shorter. Sometimes, when nests are scarce or
an accident occurs, a cuckoo is compelled to lay in any nest she can
find. Also some cuckoos are eccentric and select unusual hosts and
others fail to establish a territory and have to lay at random in a wide
variety of nests. Thus, over fifty hosts have been recorded from Britain
alone, but nevertheless, the overwhelming majority of cuckoos in this
country lay their eggs in the nests of the five or six regular fosterers
mentioned above. It is, however, not known why a female cuckoo selects
a certain specific fosterer for her initial laying, and generally continues
to select similar fosterers throughout her period of reproductive
activity. Why does a "meadow-pipit" cuckoo in Britain, for example,
regularly select the nests of meadow-pipits rather than other small birds
in which to lay her first tgg ? This is one of the unsolved mysteries of
the cuckoo's life history. One possible explanation is that she has a
strong inclination to parasitise the same species by which she herself
was reared. Much of the recent work on bird behaviour has shown that
certain sights and sounds and general situations can act as stimuli
which release inborn and well formed patterns of behaviour. Thus it is
quite possible that the plumage and song of birds exactly similar to
those which reared her and the general appearance of their nest "rings
a bell," and acts as a "releaser" of this type (habitat imprinting which
in this case might be called host imprinting), and thus stimulates the
female cuckoo to foist her eggs upon them rather than any other species.
But this is pure conjecture.

The eggs of the species as a whole are very variable both in regard
to colour and markings, but all the eggs from one individual bird are
similar. The various strains or gentes of cuckoos, such as "wagtail"
cuckoos and "pipit" cuckoos, have developed eggs which, to a greater
or lesser degree, resemble the eggs of the regular fosterers.

Many small birds have an inherited fear and dislike of the adult
cuckoo. They will mob it and drive it off in the same w^ay in which they
attack birds of prey. Pliny wrote : "They know how all birds hate them
for even very little birds are readie to war with them." Some interesting
experiments could be done with models and stuffed specimens to try to
determine by what features the cuckoo is recognised.

FFC— c

26o FLEAS, FLUKES AND CUCKOOS

If the intended foster parents surprise the cuckoo near their nest
they make frantic efforts to drive her away, buffeting and pecking her
in a courageous manner. The cuckoo never fights back — it would
certainly not be in her interest to injure the future foster parents of her
own chick — but she is very persistent and even if driven off returns
time and again and generally succeeds in laying her egg in the chosen
nest. Sometimes one or more males accompany the female and try to
divert the fosterers' attention while she quickly and furtively deposits
her egg. Chance has remarked that at times the victims behave as if
they were mesmerised by the cuckoo. Some pairs of meadow-pipits
which he had under observ^ation appeared to welcome her attentions
and seemed to fly up to her as she sat watching their activities and
"virtually invite her" to their nest. He also noted that sometimes after
a cuckoo had laid her egg the fosterers would at once begin to brood,
although their own clutch was not yet complete, as if the visitation was
regarded in the nature of an honour conferred upon them. At any rate
it can be said that the presence of the cuckoo is a disturbing and
exciting influence, which can upset the normal rhythm of their
behaviour.

A frequent result of the cuckoo's visit to a nest is its desertion by the
intended fosteiers. One of the adaptations to brood-parasitism is the
development of eggs resembhng those of the fosterers, but in the case of
the European cuckoo the adaptation is by no means perfect and the
birds often notice the strange egg and remove it, build over it or merely
abandon the nest. Some species of bird desert much more readily than
otheis and consequently keep the cuckoo at a safe distance. Many
warblers, for instance the chiffchaff and wood-warbler, will abandon
their nests if a fight has taken place, and Capek found that 77 per cent, of
cuckoos' eggs which had been placed in the nest of the latter species
were destroyed, whereas in the same district the common redstart
accepted and reared all but five per cent.

It has already been explained that the cuckoo tries to lay her egg
either before the fosterer's clutch is complete, or immediately upon
completion. In this she succeeds in about 70 per cent, of her layings.
The young cuckoo develops more rapidly than the foster nestlings and
hatches out one to four days before them if brooding had not commenced
prior to the introduction of the cuckoo's egg into the nest. Correct
timing is of great importance, for the parasite is thus given several days'
start, a definite advantage over the rest of the brood.

THE EUROPEAN CUCKOO sGl

While the young cuckoo is still blind and mute, at the tender age
of about ten hours, it develops a sudden and powerful impulse to
eHminate all the other inmates of the nest. The touch of any object,
whether it is an egg or a nestling, seems to cause it intense discomfort,
possibly even pain, and it forthwith attempts to rid itself of the intoler-
able presence. There is a small highly sensitive cavity on its back in the
region of the synsacrum into which it attempts to roll the offending egg
or nestling. Eventually, at the cost of a protracted, exhausting and hide-
ous struggle, it succeeds in hoisting its burden to the side of the nest and
ejecting it over the side. This is repeated until the young cuckoo remains
as the sole occupant of the nest. Three and a half to four days after
hatching when the plumage begins to grow, it becomes less sensitive
and the all-powerful desire for solitude fades away. The dorsal cavity,
which now no longer serves any useful purpose, is gradually obliterated.

It is a curious fact that the parent birds do not become agitated by
the disappearance of the rest of the clutch and do not appear to notice
the absence of their own young. They never attempt to feed them if
they lie starving on the ground and sometimes will even remove one
from the edge of the nest if the cuckoo has failed to heave it well over
the side — as if it were a piece of unwanted rubbish. It appears that
small passerine birds entirely fail to recognise their own young at this
stage of development if they are not in their proper place — i.e. well and
truly in the bottom of their nest.

Not all species behave like the young European cuckoo and eject
the eggs and young from the nest. In some cases, for example, in the
genus Eudynamis, the young brood-parasite is reared together with the
nestlings of the foster parents. The general colouring of the young
cuckoo's plumage somewhat resembles that of the fosterers' young —
black when crows and starlings are the host and brown if the other
nestlings are brown, too. They are consequently less conspicuous and
tone in with the rest of the brood. In another group of parasitic birds,
the African widow-birds {Vidua), this resemblance to the fosterers'
young is developed to an amazing degree — even down to such details
as the distinctive specific markings inside the gape.

When it is about twenty-one days old the young of the European
cuckoo leaves the nest, which has often, by this time, become too small
for it. Cuckoos which are reared in wrens' nests, for example, present a
most extraordinary sight bulging out of the entrance hole — often back-
side foremost. Before the young cuckoo starts on the long migration to

262 FLEAS, FLUKES AND CUCKOOS

Africa the foster parents continue to feed it for a further period of about
two weeks. This is an extremely arduous task which also incidentally
exposes them to various enemies in a manner which would not occur
with their own unobtrusive young.

Attention has already been drawn to the fact that sometimes the
female cuckoo appears to mesmerise her victims. As a nestling the
young cuckoo also produces an unusually exciting effect and not only do
the fosterers exert themselves madly to satisfy its hunger, but even strange
birds feel drawn to come and feed it. This also occurs during the period
after the young cuckoo has left the nest, but still requires feeding.
Pliny noticed this peculiar effect on the foster mother: " She joyeth to
see so goodly a bird toward : and wonders at herself that she hath
hatched and reared so trim a chick." This power of psychological
stimulation is probably yet another important biological adaptation,
which, like the extraordinary characteristics already mentioned, has
become necessaiy owing to the cuckoo's peculiar and difficult mode of
life.

Adaptation of the Cuckoo's Eggs

We have already mentioned that the colour and markings of the
cuckoo's eggs resemble, to a greater or lesser degree, those of the foster
birds chosen to rear their young. This fact has always aroused interest
and also considerable controversy. For a long time it was thought that
the female cuckoo knew the colour of her own eggs and could select a
clutch which they matched, or could, through some physiological reflex,
even control the colour of her own eggs. It has also been maintained
that the female cuckoo mates with the fosterer — a fact which, it was
claimed, explains not only the colour of her eggs but their small size, and
the derivation of the middle English term "cuckold "!

Recently, investigations, particularly painstaking observations in
the field, have thrown considerable fight on the whole problem, but it
must be admitted that uncertainty still exists concerning much of the
cuckoo's private life. Great progress was made in unravelfing the tale
when it was discovered that individual female cuckoos always lay the
same coloured eggs with the same characteristic design. Another dis-
covery which showed how selection worked was the proof obtained from
innumerable careful field studies and many experiments, that the small

THE EUROPEAN CUCKOO 263

passerine birds which are the chosen hosts recognise the cuckoo's egg
as something undesirable. Subsequently they frequently destroy it or
desert the nest in which it has been laid. It is not, of course, suggested
that the birds know the Ggg is a cuckoo's egg — what disturbs them is an
egg in some way different from their own and this sense of disharmony
prompts them to eject it or to begin to build a new nest altogether. In
these circumstances those eggs which resemble the fosterer's or vary in
the same direction, and consequently do not arouse anxiety or antag-
onism in the host, have the best chance of survival and development.
In this way selection gradually produces eggs more and more like those
of the foster parents. In the same manner elimination by natural
enemies produces plovers' eggs and terns' eggs which almost exactly
resemble the ground they nest on. In the latter case they have to be
concealed from egg thieves, while in the case of the cuckoo the host
constitutes the principal enemy. This theory, of course, assumes that
the various deviations from the original egg-type are fixed by heredity.
The genetics of the cuckoo's egg have not been investigated, but at any
rate it is known that egg-shell colour in the domestic fowl is transmitted
independently and equally by either sex. Some species of cuckoo like
the Indian hawk cuckoo {Hierococcyx varius) and all the species of the
genus Clamator, such as the red- winged crested cuckoo [Clamator
coromandus) have developed eggs which mimic the host's in every detail,
so that even an experienced ornithologist can be deceived. Sometimes the
texture of the shell or a small difference in weight reveals the truth, but
at times it is virtually impossible to tell which is the brood parasite's egg.

Such a high degree of specialisation naturally restricts the cuckoo in
question to one or two closely related species of host, which is always a
dangerous position for a parasite to adopt. The advantage of a wide
circle of fosterers probably explains why the cuckoos, once embarked
upon parasitism, diverged to hosts with eggs unlike their own, which
were primitively white or pale bluish green.

There are one or two questions which immediately spring to mind
after reading the foregoing account. It has been mentioned that some
birds are much more willing to accept the cuckoo's egg than others. The
hedge-sparrow, which we know was a favoured host in Shakespeare's
day, will brood almost anything foisted upon it from cuckoos' eggs to
pebbles. Nor does it attack the adult cuckoo. It is not surprising,
therefore, to find that as no selection takes place, no blue-type egg has
been developed by the cuckoo parasitising this species. Why then has

264 FLEAS, FLUKES AND CUCKOOS

the cuckoo not become entirely fixed to complacent fosterers? A
possible answer to this question may be that there are very few uncritical
fosterers; such birds are quickly over-parasitised and greatly reduced
in numbers and then, owing to their scarcity, the cuckoo is forced to
lay in other available nests. Therefore selection does not, in the long
run, favour the choice of uncritical hosts. It would appear that the
type of mimicry found in the European cuckoo is only developed if
fosterers exist which are neither too discriminating nor too com-
placent.

As we have seen, there are strains or "gentes" of the European
cuckoo which favour different hosts in different districts. It is assumed,
and in some cases proved, that these birds return to breed in the areas
where they were originally hatched. The strains are to some extent
isolated both geographically and ecologically. Why then has the Euro-
pean cuckoo not broken up into a number of distinct subspecies or
species ? Stresemann believes that promiscuous sexual behaviour results
in a considerable amount of crossing between the gentes, which con-
sequently works against speciation.

Colour and markings are not the only adaptations displayed by the
cuckoo's eggs. In the case of the European cuckoo, which parasitises
small birds, the eggs are relatively tiny, weighing one thirty-third only
of the parent bird. On the other hand, the great spotted cuckoo
{Clamator glandarius), a rare vagrant in Britain, which parasitises crows
and magpies, lays eggs which are larger than normal, namely one
eleventh of her own weight.

The egg shells are also heavier and tougher than those of the host's
eggs. The hasty manner in which laying takes place and the projection
into nests with side entrances, not to mention the occasional trans-
portation in the bird's beak, sets a premium on shell-toughness. It may
also prove useful in cases where the fosterers make abortive efforts to eject
the egg — for they generally begin this operation by trying to peck a
hole in it. The eggs, as in all known brood parasites, develop more
rapidly than those of their hosts.

Despite the amazing number of adaptations displayed by the
cuckoo the mortahty rate of its young is very high. Capek records that
out of 237 cuckoos' eggs laid, only 62 per cent, were hatched — but if he
could have taken into consideration those eggs which had been im-
mediately destroyed or built over by the fosterers the actual proportion
of faihires would undoubtedly have proved considerably higher.

Plate XXXVII

Whitethroat removing parasites?

a. Arctic skua: a food robber or cleptoparasite

Eric Hashing

Eric Hosking
b. Cuckoo: a brood-parasite fed by its foster-parent, a pied wagtail: this relationship

favours the transfer of parasites to new hosts
Plate XXXVIII

THE EUROPEAN CUCKOO 265

As for the young cuckoos which actually hatch, 43 per cent, die before
they are twenty days old.

It is hardly surprising, therefore, that only a small number of species
have travelled successfully along such difficult and hazardous paths and
that we find brood-parasitism is relatively a rare phenomenon among
birds. Nevertheless it has arisen independently in several unrelated
families, and is found among American starlings or hang-nests
(Icteridae), African weaver-birds (Ploceidae), honey-guides (Indicatori-
dae, which are closely related to woodpeckers), ducks (Anatidae) and
cuckoos (CucuHdae). Within the last family the habit has probably been
developed several times over as it is highly uidikely that all the parasitic
cuckoos known to-day are descended from a single parasitic ancestor.
Some knowledge of these related forms is useful for a proper under-
standing of the European cuckoo.

Brood-parasitism has probably originated in several different ways.
An important factor in the development of the habit must be the im-
pulse, manifest in a number of birds, to use or usurp the nests of other
species. In Britain it is a commonplace occurrence for sparrows to
drive out martins and swallows, and to raise their young in the vacated
nests. Stock-doves will make use of old magpies' nests and starlings
breed in cavities excavated by woodpeckers. Such examples could be
multiplied almost indefinitely.

Transitional stages between this casual seizing of other birds' nests
and the total loss of nest-building instincts can be followed in some of
the cow-birds [Molothnis). The bay- winged cow-bird {Molothrus badius)
occasionally builds her own nest and broods her own young. More
frequently she usurps the nests of other birds, which she repairs or alters
and ejects or builds over any eggs which may already be present.
Quite often several females take a fancy to the same nest and lay in it-
one female only, however, incubates the multiple clutch. A close
relative, the screaming cow-bird (M. rufo-axillaris) , has progressed
considerably farther in the same direction and is an obligate brood
parasite. The female neither builds a nest, nor takes any interest in the
welfare of her young. She lays her eggs either singly or in twos or threes
almost exclusively in the nests of her close relative, the bay- winged
cow-bird. In fact she has become dependent on the latter species for
survival and is only found within the same geographical area. In
addition to the acquired habit of usurping nests, the cow-birds manifest
a progressive weakening of the protective territorial instinct of the males.

266 FLEAS, FLUKES AND CUCKOOS

It is probably a combination of these two factors which is responsible
for the origins of brood parasitism in this genus.

Among cuckoos we find there is the same tendency. The majority of
the American species build their own rather simple nests in the forks of
trees or on the ground. One or two species, however, such as the yellow-
billed cuckoo {Coccyzus americanus) — which is a rare vagrant in Britain,
recorded in this country on about fourteen occasions — frequently usurp
other birds' nests in which they lay and incubate their own eggs.
Again others, such as the ani {Crotophagus ani) lay in mutual or com-
munal nests. Obviously, in the cuckoo family as well as in the cow-
birds, nest-seizing is an important step in the development of the para-
sitic habit, although in the case of many cuckoos there is no slackening
of the territorial instinct — at least on the part of the female bird.

Every countryman knows that a china tgg placed in a hen's nest
will encourage her to lay. It is quite possible that the parasitic habit in
certain birds originally arose from an exaggeration or perversion of this
psychological response. Thus, a female with an tgg in her oviduct, on
catching sight of an incomplete clutch, would be seized with an un-
controllable urge to lay then and there, even in another bird's nest.
Among ducks and geese, which build open nests on the ground, it is not
uncommon for two females of the same or different species to lay in one
nest — the original owner incubating and rearing the brood. At Myvatn
in Iceland, where up to twelve species of duck breed in an identical
habitat and in a similar style, there is much "adventitious parasitism"
of this type. It is particularly marked in the case of the long-tailed
duck. One South American duck {Heteronetta atricapilla) is an obligate
brood parasite, which lays her eggs principally in nests of other ducks
but also in those of various ground nesting species such as gulls, waders
and coots. It is quite likely that visual stimulation plays a big part in
determining her actions. When the brooding drive is uppermost some
gulls will attempt to "incubate" golf balls, tins or even suitably shaped
cakes if they are placed in their nests. It is, therefore, surprising that
brood parasitism is not found in this type of colonial bird. Certain
species of weaver-birds which are also colonial nesters have in fact ex-
ploited this situation. A less numerous species mingles with the main
colony and surreptitiously introduces its eggs into suitable nests.

Notwithstanding the very strong brooding instinct shown by many
birds, this drive can be easily lost if it is not maintained by natural
selection. For instance a fact with which most countrymen are familiar

THE EUROPEAN CUCKOO 267

is the difficulty experienced to-day in obtaining a broody hen. Chickens,
during the past few years, have been selected chiefly for their egg-
laying capabilities and the great majority of chicks are hatched in in-
cubators. Without deliberate intention broodiness has been "bred out"
of most strains of domestic fowls, and if by chance a broody hen is
needed to rear a covey of wild partridges, a long tour in a car from
farm to farm is required in order to locate one. The common complaint
of twenty years ago that "the hens have stopped laying and have gone
broody " is now as much a thing of the past as a sirloin of beef or a
hansom cab.

If a bird therefore embarks upon a series of chance layings in nests
other than her own, it is not difficult to see how a large number of eggs
will possess better survival value than the instinct for incubating and
brooding, and the latter characteristic will be speedily eliminated.

Most parasitic birds are sexually promiscuous, either polygamous or
polyandrous, or both. This loose way of living, particularly when
it is associated with a loss of parental instinct on the part of the male,
seems to be connected with the development of the parasitic habit. In
some cases, for example in the cow-birds, it appears as a consequence
rather than a cause of the parasitic mode of life. Further information
is required about the biology of brood-parasites, but it seems certain
that the habit is almost always associated with various types of prom-
iscuous sexual relationships.

Brood-parasites — by whatever routes they may have developed the
habit — seem to possess certain characteristics in common. Their eggs,
for example, always develop at a quicker rate than those of the host.
The advantage of hatching before the foster nestlings appears to be
extremely important, if not essential, for their survival. The European
cuckoo hatches two days before the host, and the cow-birds from one to
four days, even when the closely related species of cow-bird fosterer is
concerned. A widely spread habit among the females of brood-para-
sites is the removal or destruction of at least one egg of the foster bird.
The eggs themselves are frequently modified in certain well defined
directions. Thus, the shell is much tougher in the case of the parasite's
Ggg. This is even true of the two related cow-birds referred to above.
The size and weight of the eggs and the colour and pattern of the shell
frequently tend to resemble those of the fosterer. Some brood-parasites
lay eggs which are superficially indistinguishable from those of their
host. Well known examples of this phenomenon are recorded from

268

FLEAS, FLUKES AND CUCKOOS

weaver birds, cow-birds and cuckoos. Deliberate destruction of the eggs
or nestlings of the fosterer by the young of the brood-parasite is known
among cuckoos and honey guides. The former heave them out of the
nest and the latter are thought to peck them to death. Parasitic cow-
birds achieve the same object by a more subtle method. They manage
by importuning the foster parents to get most of the food for themselves
and the rightful young eventually die of under-nourishment and
debility.

Successful brood-parasitism, like successful ecto-parasitism, seems to
impose development and specialisation along certain lines. Therefore,
in widely separated groups of birds, located in opposite sides of the
globe we find these striking examples of parallel development.

Plate XXXIX

Eric H asking

House-martins collecting mud for their nests: a louse-fly can be seen crawling on the back

of the bird nearest the camera.

Plait XL £'« ""*'■"«

Birds congregating on the sea shore: this type of habitat and the conditions shown here
favour a high infection rate with Trematodes

BIBLIOGRAPHICAL APPENDIX

ONLY A FEW books havc been written which are concerned with the
study of parasites in general (see below) and none has been
published in this country. Moreover, the great majority of such books
are limited to the description of the parasites of man and domestic
animals, and chief stress is laid on their medical and veterinary im-
portance. The outstanding textbook of this sort is Brumpt's Precis de
Parasitologie (6th edition, Paris, 1949), which is over 2,000 pages in
length and illustrated with 1,305 text figures. It is written in the
French language. Although the book deals exclusively with the para-
sites of man, it is so comprehensive that a general idea of the morphology,
Hfe-cycles and classification of all the major parasitic groups can be
obtained from this monumental work.

There are no books in any language dealing exclusively with the
parasites of birds. The nearest approach is a recent publication edited
by Biester and Schwarte, Diseases of Poultry (Iowa, 1948). Consequently,
the general reader and the ornithologist who may now be interested are
left to struggle with the scattered hterature to the best of their ability.

In Britain, France, Germany and the United States there are
scientific periodicals devoted exclusively to parasitology — which can
be read in the hbraries of the British Museum (Natural History), the
Science Museum and the Zoological Society — and with the aid of the
subject indexes at the end of the volumes the papers dealing with bird
parasites can be sorted out and studied.

The scientific publications in such journals generally contain
references to previous papers and various books dealing with the same
subject, which helps the reader in tracking down further information.
In addition to these journals there are various publications designed
specially to assist the zoologist in keeping abreast of current literature,
pubHshed both here and abroad. These consist of classified abstracts,
classified fists of titles and authors, in conjunction with copious subject
indexes. The geographical distribution of the animals in question is

269

270 FLEAS, FLUKES AND CUCKOOS

sometimes given in detail, so that British fauna can be separated from
the rest.

There are several famous series of zoological treatises, such as the
Cambridge Natural History, which set out to survey the animal kingdom
group by group. It is of the greatest importance to consult the four
main series of this type (see below) no matter in which group of para-
sites the reader may be interested. Some of the volumes are now quite
out of date but others are recent and first class — for example, Strese-
mann's Aves (Handbuch der Zoologie, 1934).

For the study of every group of parasites it is of course useful to find
an up-to-date and reliable textbook, particularly one which supphes a
good, but not necessarily detailed, classification of the group concerned.
In many cases no such book exists and the unfortunate non-specialist is
then left to flounder. Below, the authors have endeavoured to suggest,
chapter by chapter, what literature will prove helpful if the reader
wishes to embark on a more serious study of the parasites in question.
(Unless otherwise stated the papers are written in English.) Some of the
publications have been suggested partly on account of their valuable
bibliographies, and these have been marked with an asterisk.

Throughout the text the reader will find an occasional reference to
an author or to a paper which does not appear in the relevant list in the
Bibliographical Appendix. However, the full reference to these authors
and their publications will be found in the papers indicated by an
asterisk. Thus, for Chapter 7, references to the numerous works of
Jordan and Rothschild will all be found in Pulgas by A. M. da Costa
Lima and C. R. Hathaway, A Synopsis of the British Siphonaptera by
N. C. Rothschild or Katalog der palaearktischen Aphanipteren by J. Wagner,
which contain copious bibliographies.

Most of the literary quotations in the text are so well known that it
seems unnecessary to refer to their source. The particular translations
of Pliny and Mouffet from which we have quoted so liberally are, how-
ever, especially attractive, and these references are consequently given
below.

Holland, Philemon (1601). The Historie of the World commonly called the
Naturall Historie of C. Plinius Secundus. Trans. P. Holland.

Mouffet, Thomas (1658). The Theater of Insects. English translation in
The History of Four footed Beasts and Serpents. Edited by John Rowland.

BIBLIOGRAPHICAL APPENDIX 27I

PART I

Introduction and Chapter i*

Most important periodicals concerned exclusively with

parasites
Parasitology. Cambridge 1908 —
Journal of Parasitology. Urbana, 111. 19 14 —

^eitschrift fiir Parasitenkunde. Berlin 1928 — (chiefly in German).
Annales de Parasitologic humaine et comparie. Paris 1922 — (chiefly in French).
Rivista de Parassitologia. Rome 1937 — (chiefly in Italian).
1[ Experimental Parasitology. New York 1952 —

Most useful abstracts and indexes (in English) for use by

the parasitologist

Zoological Record. London.

Biological Abstracts. Philadelphia.

Review of Applied Entomology. (Series B) Medical and Veterinary. London.

Helminthological Abstracts. St. Albans, England.

Main Zoological Treatises
Cambridge Natural History. London.

Handbuch der ^oologie {Kiikenthal und Krumbach) (in German).
Bronns Klassen und Ordnungen des Tierreichs. Leipzig (in German).
Traite de ^oologie. Paris (in French).

General books on parasitism
Baer, J. G. (1946). Le Parasitisme. Lausanne (in French).
Baer, Jean G. (1951). Ecology of Animal Parasites. University of Illinois

Press, Urbana.
Brumpt, E. (1949). Precis de Parasitologic. Paris (in French).
Gaullery, M. (1922). Le Parasitisme et la Symbiose. Paris (2nd edition,

1950) (in French).
*Chandler, a. C. (1930). Introduction to Parasitology. (9th edition). Revised

1955. London and New York.
Grasse, p. p. (1935). Parasites et Parasitisme. Paris (in French).
Hegner, R. W., Root, F. M., Augustine, D. L. and Huff, C. G. (1938).

Parasitology. New York.
Lap age, Geoffrey (1951). Parasitic Animals. Cambridge Library of

Modern Science.
Pearse, a. S. (1942). Introduction to Parasitology. Springfield, 111.
Riley, W. A. (1945). Introduction to the Study of Animal Parasites and Para-
sitism. Minneapolis.

t All items thus marked have been added in the third edition (1957).

272 FLEAS, FLUKES AND CUCKOOS

Books on the bird host
♦BiESTER, H. E. and Schwarte, L. H. (1943). Diseases of Poultry. (2nd

edition). Revised 1948. Iowa, U.S.A.
Catalogue of the Birds in the British Museum. 27 vols. London.
|Grasse, Pierre-P. (editor) (1950). Oiseaux. Traite de ^oologie, XV. Paris

(in French).

Peters, J. L. (1931 — ). Clieck-List of Birds of the World. Cambridge, Mass.
Romanoff, A. L. and A. J. S. ( 1 948) . The Avian Egg. London and New York.
Stresemann, E. (1927- 1 934). Aves : in Kiikenthal and Krumbach, Hand-
buch der Zoologie. Bd. 7, Hft. 2. Berlin and Leipzig (in German).

WiTHERBY, H. P., JOURDAIN, F. R. C, TiCEHURST, N. F., TuCKER, B. W.

(1938- 1 941). The Handbook of British Birds. Vols. I-V. London.

Note : The lists of parasites given for each species of bird in Niethammer's
Handbuch der deutschen Vogelkunde I-II, Leipzig 193 7- 1938 is totally un-
reUable and it is best to ignore this part of the publication. An accurate
compilation of records of the parasites of British birds — providing that in
all cases the source of the record is given — would be quite invaluable.

Chapters 2 and 3. Commensalism and Symbiosis

There are no books which deal specifically with commensalism and
symbiosis among birds, but the following papers should be consulted and
the various references listed in their respective bibliographies should
also be read and studied. If added information is required about
particular species of birds, for instance the buff-backed heron, or the
sheath-bills, it is advisable to consult accepted ornithological authorities
such as Bannerman {Birds of Tropical West Africa^ Vols. I-V, London,
1930), or Murphy [Oceanic Birds of South America, Vols. I & II, New York,
1936). One or two papers have been published recently dealing specifi-
cally with the peculiar habit known as phoresy.

Commensalism and Symbiosis
•j-Allee, W. C, Emerson, A. E., Park, O., Park, T., and Schmidt, K. P.

(1949). Principles of Animal Ecology. 837 pp. Saunders, Philadelphia.
*Baker, E. C. Stuart (1931). Nesting associations between birds and

wasps, ants or termites in the Oriental Region. Proc. Ent. Soc. London,

6: 34-37-
BucHNER, P. E. C. (1930). Tier und Pflanze in Symbiose. Berlin (in German),
f Davenport, Demorest (1955). Specificity and behavior in symbioses.

The Quart. Rev. of Biol., 30: 29-46.
|Durango, S. (1949). The nesting associations of birds with social insects

BIBLIOGRAPHICAL APPENDIX 273

and with birds of different species. Extracted and translated in Ibis, gi:

140-143.
Fisher, J. and Hinde, R. A. (1949). The Opening of Milk-bottles by Birds.

British Birds, 42 : 347-357-
Harvey, E. N. (1940). Living Light. Pp. xvi + 328 col. frontisp. and

88 figs. Princeton.
Lynes, H. and Vincent, J. (1939). The White-rumped Swift M. coffer

beginning to breed under the eaves of houses. Ostrich (Pretoria), 10 :

75-S4-
MoREAu, R. E. (1933). The food of the Red-billed Oxpecker, Buphagus

erythrorhynchus (Stanley). Bull. Ent. Res. London^ 24: 325-335.
*MoREAu, R. E. (1942). The nesting of African Birds in association with

other Hving things. Ibis. (14), 6 : 240-263.
Myers, J. G. (1935). Nesting associations of Birds with social insects.

Trans. Ent. Soc. London, 83 : 11-22.
Nelson, T. H. (1882). Small birds carried by Cranes in their migrations.

The Zoologist, 60 : 73.
Supplement to the report of the twelfth annual meeting of the American

Society of Parasitologists. Report of the Committee (1937). Journal of

Parasitology, 23 : 325-32g.

See also The Handbook of British Birds (Witherby) under the individual
species referred to in the text.

Phoresy
fBEQUAERT, J. C. (1953). The Hippoboscidae or Louse-flies (Diptera) of

Mammals and Birds. Ent. amer.j 32: 163-174.
fSMiT, F. G. A. M. (1953). Transport of Mallophaga by Fleas. Parasitology,

43' 205-206.
Vachon, M. (1947). Nouvelles remarques a propos de la phoresie des

Pseudoscorpions. Bull. Mus. Hist. Nat. (2), Paris (in French), ig : 84-87.
Warburton, C. (1928). Ornithomyia avicularia (Diptera Hippoboscidae) as

the carrier of Mallophaga, with some remarks on phoresy in insects.

Parasitology (Cambridge), 20 : 175-178.

Chapters 4, 5 and 6

The Effect of Parasites on the Host

The Effect of Parasitism on the Parasite

The Origins of Parasitism and the Evolution of Parasites

Relevant material will be found in all the books on the general
aspect of parasitism quoted above. The following publications should
also prove interesting.

274 FLEAS, FLUKES AND CUCKOOS

Ball, G. H. (1943). Parasitism and evolution. Amer. Nat. yy : 345-346.
IBecker, Elery R. (1953). How parasites tolerate their hosts. Journal of

Parasitology, 3g: 467-480.
Bodenheimer, F. S. (1938). Problems of Animal Ecology. Oxford.
Evolution, Essays on Aspects of Evolutionary Biology (1938), Edited by G. R.

de Beer. Oxford.
Elton, C. S. (1930). Animal Ecology and Evolution. Oxford.
GiARD, A. (1911-1913). Oeuvres diverses (2 Vols.). Paris (in French).
GoLDSCHMiDT, R. (1940). The Material basis of Evolution. California and

London.
Haldane, J. B. S. (1932). The Causes of Evolution. London.
Huxley, J. S. (1940). The New Systematics. Oxford.
*HuxLEY, J. S. (1942). Evolution, The Modern Synthesis. London.
|Lack, David (1954). The Natural Regulation of Animal Numbers, 343 pp.

Oxford.
Mayr, E. (1942). Systematics and tJie Origin of Species . . . New York.
Metcalf, M. M. (1929). Parasites and the aid they give in problems of

taxonomy, geographical distribution and paleogeography. Smithson.

Misc. Pub I. 81. No. 8.
Rothschild, N. C. (191 7). Convergent development among certain

ectoparasites. Proc. Ent. Soc. (London), igiy : 141 -156.
Shipley, A. E. (1926). Parasitism in evolution. Sci. Progr. (London), 20:

pt. H, 632-661.
Smith, Theobald, (1934). Parasitism and Disease. Princeton.
Stunkard, H. W. (1929). Parasitism as a biological phenomenon. Scient.

Monthly i 28 : 349-362.

PART II

Introduction and Chapters 7 and 8
Fleas and Feather Lice

In order to study any particular order of insects it is necessary to
have at hand certain books dealing with general entomology. For-
tunately, several first class textbooks on the Insecta have been written
in English.

Fleas (Aphaniptera) : A satisfactory classification of the families
will be found in Hopkins & Rothschild (1953). An Illustrated Catalogue
of the Rothschild Collection of Fleas [Siphonaptera) in the British Museum
{Natural History), I, but in this first volume only the Pulicoidea are
dealt with in detail. The species of purely economic interest are

BIBLIOGRAPHICAL APPENDIX 275

adequately classified by Jordan in Smart's Insects of Medical Importance.
The external morphology of the flea is admirably dealt with by
Snodgrass, 1945 (see below). With regard to the fauna of Britain, the
most up-to-date paper is still that of Rothschild published in 191 5, but
shortly a section by F. G. A. M. Smit dealing with fleas will appear in
the series Handbooks for the Identification of British Insects, published by
the Royal Entomological Society of London. This will save the
unfortunate beginner a hunt through the papers Hsted in biblio-
graphies and a search through the Zoological Record for British records.
Feather hce (Mallophaga) : There is no satisfactory classification of
the feather Hce in existence. The best account of their biology will be
found in Hopkins' paper which deals principally with the Mallophaga
of mammals. It has an excellent bibliography.

General Entomology

Brues, C. T. (1946). Insect Dietry. An account of the food habits of insects.
Cambridge, Mass. Harvard Univ. Press.

Ford, E. B. (1945). New Naturahst Series, i. Butterflies. London.

Imms, a. D. (1925). A General Textbook of Entomology. (3rd edition, revised
1934) London.

Imms, A. D. (1947). New Naturalist Series, 8. Insect Natural History. London.

Smart, J. (1943). A Handbook for the Identification of Insects of Medical Import-
ance, with chapters on fleas by K. Jordan and arachnids by
R. J. Whittick. London. Brit. Mus. (Nat. Hist.). Revised edition 1948.

Snodgrass, R. E. (1935). Principles of Insect Morphology. New York and
London.

♦Steinhaus, E. a. (1946). Insect Microbiology. New York and London.

*WiGGLESWORTH, V. B. (1939). The Principles of Insect Physiology. (3rd
edition 1947). London.

Fleas (Aphaniptera)
Allan, Ronald M. (1950). Fleas (Siphonaptera) from birds in North-East

Scotland. The Scottish Naturalist, 62 : 33-41.
Buxton, P. A. (1932). Studies on the biology of fleas. London Naturalist,

1932 : 39-42.
Buxton, P. A. (1932). The climate in which the rat-flea Hves. Ind. Jour.

Med. Res. 20 : 28i-2gy.
Buxton, P. A. (1938). Quantitative sindi^s, on th^hiolo^ o^ Xenopsyllacheopis

(Siphonaptera). Ind. Jour. Med. Res. 26 : 505-530.
*GosTA LIMA, A. M. da^ and Hathaway, G. R. (1946). Pulgas. Monografias

do Instituto Oswaldo Cruz. Rio de Janeiro, Brasil. (This paper contains a

most important bibliography).

FFC— T

276 FLEAS, FLUKES AND CUCKOOS

fDuNNET, G. M., & Allan, R. M. (1955). Annual and regional variation
in the flea populations of nests of the house-martin Martula u. urbica (L.)
in North-east Scotland. Ent. mon. Mag., gi: 161-167.

Hirst, L. F. (1925). Plague Fleas, with special reference to the Milroy
Lectures, 1924. Jour. Hyg. 24 : 1-16.

jHoPKiNS, G. H. E., & Rothschild, M. (1953). An Illustrated Catalogue of
the Rotlischild Collection of Fleas (Siphonaptera) in the British Museum {Natural
History) y i, London.

loFF, L G. (1941). The ecology of fleas in connection with their epidemio-
logical importance. Pyatigorsk. Ordzhonik Kraev. Izd. 116 (in Russian).

Jordan, K. (1926). On Xenopsylla and allied genera of Siphonaptera.
Verh. III. Internat. Ent. Kongr. (Zurich), 1925: ^q^-62y.

Jordan, K. (1929). On some problems of distribution, variability and
variation in North American Siphonaptera. Trans. 4th Int. Cong, of Ent.
(Ithaca, 1928), 48g'4gg.

Jordan, K. (1942). On Parapsyllus and some closely related genera of
Siphonaptera. Eos. (Madrid), 18 : y'2g.

Mitzmain, M. B. (19 10). Some new facts on the bionomics of the California
rodent fleas. Ann. Ent. Soc. Amer. 5 ; 61-82.

*Rothschild, N. C. (19 15). A synopsis of the British Siphonaptera. Entom.
Mag. (London), 5/; 4g-ii2. (important references for early records).

Rothschild, M. (1948). Bird fleas collected by Miss Theresa Clay, Colonel
Richard Meinertzhagen and Captain W. H. Pollen in the Island of
Ushant, Brittany, France, with a Note on the Distribution of Cerato-
phyllus borealis Rothschild (1907). Entom. 81 : 84-gj.

Rothschild, M. (1951). A collection of fleas from the bodies of British
birds, with notes on their distribution and host preferences. Bulletin of
the British Museum {Natural History), Entomology, 2: no. 4, in press.

■fRoTHscHiLD, M. ( 1 955) . The distribution of Ceratophyllus borealis Rothschild,
1906, and C.garee Rothschild, 1902, with records of specimens intermediate
between the two. Trans. Royal Ent. Soc, loy: 295-317.

Sharif, M. (1936). The Life history, the biology and the anatomy of the
early stages of the rat-flea, Nosopsyllus fasciatus, Bosc. Abstr., Diss. Univ.
Cambridge : 2g-jo.

|Smit, F. G. a. M. (1954). Lopper. Danmarks Fauna 60: 125 pp. Copen-
hagen. (In Danish).

jSmit, F. G. a. M., and Allan, R. M. 1955. Variation in the seventh
sternum of females of the House-Martin flea Ceratophyllus farreni Roths-
child, with remarks on synonymy. The Entomologist, 88 (iioi): 41-46.

ISmit, F. G. a. M., and Rothschild, M. (1955). Two new subspecies of
fleas (Siphonaptera) from the British Isles, with a discussion on their dis-
tribution. Trans. Royal Ent. Soc, ioy\ 341-372.

BIBLIOGRAPHICAL APPENDIX 277

Snodgrass, R. E. (1946). The Skeletal Anatomy of fleas (Siphonaptera),

Smithson Misc. Coll. 104 : no. 18, i-Sg.
Strickland, D. (19 14). The biology of Ceratophyllus fasciatus Bosc, the

common rat-flea of Great Britain. Jour. Hyg. 14 : I2g-i42.

* Wagner, J. (1930). Katalog der palaearktischen Aphanipteren. Vienna :

F. Wagner, ^j. (The subsequent additions to this catalogue must not be

overlooked) .
Wagner, J. (1939)- Aphaniptera. In Bronns Klassen und Ordnungen des

Tierreichs, Vol. 5, Abt. 3, Buch 13, Teil f, 114.
Waterston, J. (19 10). On some habits and hosts of bird Ceratophylli

taken in Scotland in 1909; with description of a new species (G. roths-

childi) and records of various Siphonaptera. Proc. Roy. Phys. Soc. Edin.

188: 73-gi.
Wigglesworth, v. B. (1935). The regulation of respiration in the

Hea, Xenopsy Ha cheopis Roths. (Pulicidae). Proc. Roy. Soc. 118: 397-419-

Feather lice (Mallophaga)
Ghisholm, a. H. (1944). The problem of "Anting." Ibis, 86: 389-405,
Denny, H. (1842). Monographia Anoplurorum Britanniae. London.
GiEBEL, G. G. (1874). Insecta Epizoa. Leipzig, (in German).

* Hopkins, G. H. E. (1949). The host-associations of the lice of mammals.

Proc. Z^ol. Soc. London, 119 : 387-604.
Hopkins, G. H. E. and Clay, T. (1952). A check-list of the Mallophaga.

British Museum (Natural History).
*Keler, S. (1938). Ubersicht iiber die gesamte Literatur der Mallophagen.

Z' angew. Ent. 25 : 487-524.
PiAGET, E. (1880). Les Pediculines. Leyden. (in French).
Piaget, E. (1885). Les Pediculines. Supplement. Leyden. (in French).
Redi, F. (1668). Esperienze intorno alia generazione degli insetti fatti. Florence.

(in Italian).

PART III

Chapter 9, Protozoa

Wenyon's textbook is an all time classic. Although necessarily out
of date in certain respects (for example, further important discoveries
have been made concerning the life-cycle of malaria during the last few
years), it can still form the basis of any research on the Protozoa. Bird
Malaria (although the host check list is unreliable), is a book which
should also be read in conjunction with this chapter.

278 FLEAS, FLUKES AND CUCKOOS

jBaker, J. R. (1955 personal communication: part in press). The blood

protozoa of British birds.
I Buxton, P. A. (1955). The Natural History of Tsetse Flies, 816 pp., 47 pis.,

London.
Coles, A. C. (19 14). Blood parasites found in mammals, birds and fishes

in England. Parasitology, 7 .• ly.
Hewitt, R. (1940). Bird Malaria. Amer. Hygiene Monogr. Ser. No. 15.

Baltimore.
Huff, Clay G. and Coulston, Frederick. (1944). The development of

Plasjiiodium gallinaceum from sporozoite to erythrocytic trophozoite.

J. Infect. Dis. 75 : 231-249.
James, S. P. and Tate, P. (1938). Exo-erythrocytic schizogony in Plas-
modium gallinaceum Brumpt. 1935. Parasitology, 30: 128-ijg.
James, S. P. (1939). The incidence of exo-erythrocytic schizogony in

Plasmodium gallinaceum in relation to the mode of infection. Trans.

Roy. Soc. Trop. Med. and Hyg. 32 : jS^-yGg.
Kudo, R. R. (1946). Protozoology. (3rd edition). Springfield, 111.
Shortt, H. E., Menon, K. P. and Seetharama Iyer, P. V. (1940). The

forms of Plasmodiwn gallinaceum present in the incubation period of

the infection. Ind. J. Med. Res. 28 : 2^3-2^6.
Wenyon, C. M. (1926). Protozoology. Vols. I and II. London.

Chapter 10, Worms (Vermes)

There is no textbook in the English language concerned with para-
sitic worms as a whole. Sprehn's Lehrbuch der Helminthologie, a German
publication, deals with all four main groups and is the best of its kind.
Various medical and veterinary helminthologies are however available,
several of which are written in English. The worms as a whole com-
prise an enormous group and it is preferable to consider the various
classes separately. Unfortunately no satisfactory classification of the
flukes has been compiled up to date. The tapeworms and roundworms
are admirably dealt with by Fuhrmann and the Chitwoods. Since
Meyer's monograph on the spiny-headed worms, van Cleave has
suggested a modified classification and the reader is advised to hunt up
his various papers on this group which have the advantage of being
written in English. Two lists of helminths by Baylis from British verte-
brates are very useful. One of the most urgent requirements in the
field of helminthology is a compilation describing the known life-
cycles of parasitic worms, together with lists of their intermediate hosts.

BIBLIOGRAPHICAL APPENDIX 279

General books and papers on Worms
Baylis, H. a. (1928). Records of some Parasidc Worms from British

Vertebrates. Ann. Mag. Nat. Hist. (10), / ; 32g-j4j.
Baylis, H. A. (1939). Further records of Parasitic Worms from British

Vertebrates. Ann. Mag. Nat. Hist. (11), 4: 4y;^.
I Brand, Theodor Von (1952). Chemical Physiology of Endoparasitic Animals,

339 PP" New York.
DoLLFUS, R. P. (1946). Parasites (animaux et vegetaux) des Helminthes.

Encyclopedie Biologique. 27. Paris, (in French).
Faust, E. C. (1929). Human Helminthology ; a Manual for Clinicians, Sanitarians^

and Medical Zoologists. Philadelphia and London.
Neveu-Lemaire, M. (1936). Traite d'helminthologie mSdicale et veterinaire.

Paris, (in French).
Sprehn, G. E. W. (1932). Lehrbuch der Helminthologie. Eine Naturgeschichte

der in deutschen S'augetieren und Vbgeln schnarotzenden Wiirmer unter beson-

derer Berucksichtigung der Helminthen des Menshen, der Haustiere und wichtigsten

Nutztiere. Berlin, (in German).

Roundworms (Nematoda)
Chitwood, B. G. and M. B. (1937 — last published 1948). An introduction

to nematology. Baltimore (Monumental Printing Co.) Washington, D.C.

(A good skeleton classification will be found in Part I, Section i, p. 49).
Cram, E. B. (1927). Bird parasites of the Nematode suborders Strongylata,

Ascaridata and Spirurata. Bull. U.S. Nat. Mus. 140 : 1-465.
Dougherty, Ellsworth C. (in press). Evolution of zooparasitic groups

in the phylum Nematoda, with special reference to host-distribution.

Journal of Parasitology , 57 ; no. 4.

Spiny-headed worms (Acanthocephala)
Meyer, A. (1933). Acanthocephala. Bronns Klassen u. Ordnungen des Tierreichs
Leipzig. 4 (Abt. 2 Buch 2 Lfg. 2) 333-582. (in German).

Tapeworms (Gestoda)
f Baer, Jean G. (1954). Revision taxinomique et etude biologique des

Cestodes de la famille des Tetrabothriidae. Memoires de VUniversite de

Neuchatel, i, 121 pp. Neuchatel (in French).
Fuhrmann, O. (1931). Vermes Aniera. Cestoda. in Kiikenthal und Krumbach.

Handbuch der Zool. 2, Teil 2. Berlin, 25y-4i6. (in German).
Fuhrmann, O. (1932). Les tenias des oiseaux. Mem. Inst Univ. Neuchatel

8: I -38 1. 147 figs, (in French).
Larsh, John E. (1951). Host-parasite relationships in cestode infections,

with emphasis on host resistance. Journal of Parastology, 3J : no. 4,

343-352.

280 FLEAS, FLUKES AND CUCKOOS

Flukes (Trematoda)
Dawes, B. (1946). The Trematoda. Cambridge.
FuHRMANN, O. (1928). Trematoda. In Kukenthal und Krumbach, Hand-

buch d. Zool. Berlin, 2, Part 2. 1-140. (in German).
Larue, George R. (in press). Host-parasite relations among the digenetic

trematodes. Journal of Parasitology , 57 ; no. 4.
fNicoLL, W. (1923). A reference list of the trematode parasites of British

birds. Parisitology, /j ; Jji-202.

Leeches (Hirudinea)
I Mann, K. H. (1954). A key to the British Freshwater Leeches with notes on their

ecology. Freshwater Biological Association Scientific Publication No. 14,

21 pp.
|Mann, K. H. (1955). The Ecology of the British Freshwater Leeches.

The Journal of Animal Ecology: 24, (i): 98-119.
Harding, W. A. (1910). A revision of the British Leeches. Parasitology^

J : 1J0-201.

Chapter ii, Flies (Diptera)

Apart from the general books on insects, the volumes mentioned
below are of great assistance and have provided most of the data for
this chapter. Bequaert's monograph on the louse-flies is a masterpiece,
and Seguy provides useful lists in both his papers. Mattingly's paper
is invaluable for the determination of the mosquitoes.

*Bates, Marston, (1949). The Natural History of Mosquitoes. New York.
fBEQUAERT, Joseph C. (1953). The Hippoboscidae or Louse-flies (Diptera)

of Mammals and Birds. Part i : Structure, Physiology and Natural

History. Entomologica Americana, 32 (new series): 1-209, ^33' 211-442.
|CoE, R. L., Freeman, Paul, & Mattingly, P. F. (1950). Handbooks for

the identification of British Insects, IX, part 2, Diptera 2. Nematocera :

families Tipulidae to Chironomidae : pp. 1-2 16, London.
Edwards, F. W., Oldroyd, H., & Smart, J. (1939). British Blood-sucking

Flies. London.
Keilin, D. (1924). On the Life-history of Anthomyia procellaris Rond, and

A. pluvialis L., hibernating in nests of birds. Parasitology, 16 : 150-159.
Marshall, J. F. (1938). The British Mosquitoes. London.
I Oldroyd, H. (1949). Handbooks for the identification of British insects, IX,

part I, Diptera i. Introduction and key to families : pp. 1-49. London.
Seguy, E. (1946). Dipt^res ornithophiles in Encycl. Ent. Ser. B 2, 10 : 1 18-132

(in French).

t This list refers to records from birds on the British list, not British birds, as the
title suggests.

BIBLIOGRAPHIPAL APPENDIX 281

f Seguy, E. (1950). La Biologic des Dipteres. Encycl. ent. Ser. A, 26, 609 pp.

(in French).
|Tate, p. (1954). Notes upon the biology and morphology of the immature

stages o{ Neottiophilum praeustum (Meigen, 1926) (Diptera: Neottiophilidae)

parasitic on birds. Parasitology ^ 44: 1 11- 119.

Chapter 12, Mites and Ticks (Agarina)

The recent French publication Traiti de ^oologie (see below), gives a
good general account of the mites and ticks, in French, a useful
classification (p. 879), and a selected bibliography. One of the outstand-
ing contributions to the knowledge of ticks is Nuttall's and Warburton's
series of papers. Portions of the monograph are necessarily out of date
but nevertheless it should be read from cover to cover. A magnificent
monograph on the Analgesoidea (feather mites) has been published by
Dubinin, unfortunately in Russian. Recent papers on British ticks can
be found in Parasitology. Various papers on parasitic mites have been pub-
lished by Turk (in English) and the reader is advised to look these up.

Heymons' monograph on the tongueworms (Pentastomida) is first
class. Unfortunately it is in German and there is no equivalent in English.

* Andre, M. (1949). Ordre des Acariens. Grasse Traiti de ^oologie. Tome 6:

yg5-8g2, Paris (in French). (A useful classification will be found on p. 879).
f Baker, E. W., & Wharton, G. W. (1952). An Introduction to Acarology,
465 pp.. New York.

* Heymons, R. (1935). Pentastomida. Bronns Klassen und Ordnungen des

Tierreichs. Bd. 5, Abt. IV. Buch i. Leipzig (in German).
NuTTALL, G. H. F., Warburton, C., Cooper, W. F. and Robinson, L. E.

(1908- 1 926). Ticks, A Monograph of the Ixodoidea. Pts. 1-4, London.
jRadford, Charles D. (1949-50). The mites (Acarina) parasitic on

mammals, birds and reptiles. Parasitology, 40 : 366-394.
j- Radford, Charles D. (1952-53). The mites (Acarina : Analgesidae)

living on or in the feathers of birds. Parasitology, 42: 199-230.
Vitzthum, H. Graf (1929). Milben, Acari. Tierwelt Mitteleuropas Bd. IIL

Lfg. 3. (in German).

Chapter 13, Micro-Parasites

Bacteria and Viruses : Topley and Wilson's textbook is the all-time
classic in this field, and in every respect is beyond praise. (For a
classification of bacteria see Vol. I, p. 310). Various pertinent chapters
in the Diseases of Poultry (see above) are also useful especially for tracking
down obscure papers.

282 FLEAS, FLUKES AND CUCKOOS

Fungi. The best available textbooks dealing with fungi are in
French (see below). The species described in Dollfus' compilation are
of the greatest interest in view of the importance of the nematode
parasites of birds.

Brumpt, E. (1949). Precis de parasitologie. Vols. I and II. Paris, (for fungi

see pp. 1607-2039). (in French).
Dane, Surrey D. (1948). A disease of Manx Shearwaters {Pufflnus puffinus).

J. Animal Ecol. ly : 158-164.
DoLLFUS, R. (1946). Parasites (animaux et vegetaux) des Helminthes.

Encyclopedie Biologique. Paris.
Florey, H. W., Chain, E., Heatley, N. G., Jennings, M. A.^ Sanders,

A. G., Abraham, E. P. and Florey, M. E. (1949). Antibiotics. A survey

of Penicillin, Streptomycin, and other antimicrobial substances from fungi, acti-

nomycetes, bacteria, and plants. 2 Volumes. Oxford University Press,

London, New York and Toronto.
Gardner, A. D. (1931). Microbes and Ultramicrobes. London.
Langeron, M. (1945). Precis de mycologie. Paris, (reprinting, new edition

promised for 1950).
•fPouLDiNG, R. H. (1952). Five cases of Aspergillosis in Immature gulls.

Ibis: g4, No. 2, pp. 364-366.
Smith, K. M. (1940). The Virus; Life's Enemy. Cambridge (reprinted

with appendix 1948).
*ToPLEY, W. W. C. and Wilson, G. S. (1929). Principles of Bacteriology

and Immunity. (3rd edition). Revised by G. S. Wilson and A. A. Miles

1946 (in two vols.), London.
Urbain, a. and Guillot, G. (1938). Les aspergilloses Aviaires. Rev. Path.

Comp. Hyg. Gen. no. 503, 2y pp. (in French).

Chapter 14, The Fauna of Birds' Nests

There are, unfortunately, no general papers in English dealing with
the fauna of birds' nests, and it is to be hoped that someone will soon
supply the missing volume. Large numbers of scattered papers in
various entomological journals (such as the Entomologists^ Monthly
Magazine, the Entomologist, etc.) contain isolated records of beetles,
flies, fleas and other insects from nests of British birds, but an up-to-
date comprehensive review covering all the groups concerned is
urgently required. Chapter 14 has been compiled from both published
and unpublished notes generously supplied by Mr. Basden, Dr. China.
Mr. Donisthorpe, Dr. Hinton, Mr. Spittle and Dr. Turk.

The following publications should prove useful :

BIBLIOGRAPHICAL APPENDIX 283

I Armstrong, E. A. (1953). Nidicoles and Parasites of the Wren. Irish Nat. J.

II : 57-64.
Heim de Balsac, H. (1938). Commensalisme ornithophile de Coleopt^res

Staphylinides; son determinisme par exigences thermiques de maturation

des gonades. C.R. Acad. Sci. Fr.j (Paris), 2oy : 644-646. (in French).
HiNTON, H. E. (1945). A Monograph of the Beetles associated with Stored Products.

Vol. I. London.
Johnson, C. G. (1939). Taxonomic characters, variability and relative

growth in Cimex lectularius L. and C. columbarius J enyns (heteropt. Cimicidae)

Trans. R. Ent. Soc. (London), 8g : 543-568.
Joy, N. H. (1932). A practical handbook of British beetles. London. 2 vols.
NoRDBERG, S. (1936). Biologisch-oiklogische Untersuchungen Uber die

Vogelnidicolen. Acta J^oologica Fennica 21, Helsingfors. (in German).
Ogilvie, C. M. (1949). Observations in a rookery in winter. Brit. Birds,

42 : 65-68.
Seguy, E. (1946). Dipteres ornithophiles ivi Encycl. Ent. Set. B2y 10: 1 18-132,

(in French).
tUsiNGER, R. L., & Ferris, G. F. (in press). The Family Cimicidae {Hemiptera

Heteroptera) .

Chapters 15 and 16, Skuas and Cuckoos

The account of the skuas is taken principally from the chapter
relating to this group in Witherby and chapter 1 6 is based entirely upon
Stresemann's account of the cuckoo. The latter is probably the best
short summary up to date (see below). The other books mentioned in
the bibliography should be read and studied since they give a good
picture of the field work carried out in connection with the cuckoo.
Mr. H. N. Southern has kindly allowed us to read some notes from his
paper on the European cuckoo which should be published shortly.

Skuas
Meinertzhagen, R. (1941). August in Shetland. Ibis^ 5 : 105-iiy.
Murphy, R. C. (1936). Oceanic Birds of South America. Vols. I and II.

American Museum of Natural History. New York. (pp. 1006- 1033 for

Stercorariidae).
Witherby, H. F., Jourdain, F. R. C, Tigehurst, N. F., and Tucker,

B. W. ( 1 94 1) . Handbook of British Birds. Vol. V. (pp, 122-137, for Stercorarius) .

Cuckoos
Baker, E. C. S. (1942;. Cuckoo problems. London.
Chance, E. P. (1940). The truth about the Cuckoo. London.

284

FLEAS, FLUKES AND CUCKOOS

Friedmann, H. (1928). Social parasitism in birds. The Quart. Rev. of Biol.

(Baltimore), 5; 554-56g.
Friedmann, H. (1948). The parasitic cuckoos of Africa. Washington Academy

of Science, Monogr. No. i .
♦Stresemann, E. (1927-1934). Aves : in Kukenthal and Krumbach,

Handbuch der Zoologie, Berlin and Leipzig, (pp. 417-427 and 818-819

for Cuculidae). (in German).
Thorpe, W. H. (1945). The evolutionary significance of habitat selection.

J. Anim. Ecol. 14 : i6y-iyo.

INDEX OF POPULAR AND
SCIENTIFIC NAMES

Acanthocephala, see Spiny-
headed Worms
Acarina, see Mites
Achorion (Fungi), 242
Acoleiis vaginatus (Tapeworm) ,

194
Actinomyces rhodnii (Fungus),

20
Actornithophilus (Feather

Lice), 121, 133
Actornithophilus patellatus, see

Curlew Quill Louse
Acuaria (Roundworms), 184
Acuaria hamulosa (Gizzard

Worm), 185
Acuaria laticeps

(Roundworm), 184
Acuaria spiralis

(Roundworm), 185
Aedes (Mosquitoes), 214,

PI. XXX (211)
Aedes geniculatus (Mosquito),

165
Alaudidae (Larks), 165
Alcedoecus (Feather Lice), 150
Alcedoffula (Feather Lice), 150
Aleochara (Rove Beetles), 249
Alethe (Thrushes), see Ant-
birds
Alpine Chough {Pyrrhocorax

graculus), 89, 95
Alpine Hare {Lepus timidus),

87,.89
Amabilia (Tapeworms), 194
Ambiycera (Feather Lice),

Main Sections are in heavy type

122, 123, 132, 139,

147-156, PL XXII (131)
American Sand-Martin Flea

(Ceratophyllus riparius), 86
American Wigeon {Anas

americana), 253
Amoebidae (Protozoa), 174
Amphibians, 161, 188
Amyrsidea (Feather Lice), 156
Analges chelopus (Mite), 225,

PL XXXI (226)
Analgesidae, see Feather

Mites
Anas americana, see American

Wigeon
i4«<3/zVo/a (Feather Lice), 132,

141
^nato^fiAf (Feather Lice), 132,

141

Ancistrona (Feather Lice),
128, 153

Anodonta (Freshwater Mus-
sels), 30

Anomotaenia (Tapeworms),

193

Anomotaenia arionis (Tape-
worm), 194

Anomotaenia constricta (Tape-
worm), 193

Anomotaenia nymphaea (Tape-
worm), 194

Anopheles (Mosquitoes), 214

Anoplocephalidae (Tape-
worms), 197

Anoplura, see Sucking Louse

Anseriformes (Ducks, Geese,

Swans), 43, 130, 131, 141,

152-153, 163, 174, 183,

i95> i99> 205

Ant-birds {Alethe), 254

Anthocorid Bug {Lyctocoris

campestris), 248
Anthomyia (Flies), 251
Ants, 13, 14, 25, 26, 49, 50,
51. 55> J03» 126-128, 197,
254
Apatemon gracilis (Fluke), 206
Aphaniptera, see Fleas
Aploparaksis filum (Tape-
worm), 195
Aploparaksis furcigera (Tape-
worm), 195
Apodiformes (Swifts), 150
Aporina delafondi (Tape-
worm), 197
Aponomma sp. (Tick), fig.

P- 234
Aquanirmus (Feather Lice),

153
Arctic Fox, 194

Arctic Hare, 92

Arctic Skua {Stercorarius para-
siticus), 15, no, 213,
254, 255, PL XXXVIII
(265)

Arctic Tern {Sterna macrura),

15. 135
Ardeicola (Feather Lice), 152
Ardeiphilus (Feather Lice),

15a

INDEX TO POPULAR AND SCIENTIFIC NAMES

285

Argas (Ticks), 238

Argas reflexus, see Pigeon Tick

Argas persicus, see Fowl Tick

Argasidae (Ticks), 39, 229,
231

Armadilliiim vulgar e, see Wood
Louse

Armillifer armillatus (Tongue-
Worm), 233

Arthropods, 19, 48, 63, 150,
163, 172, 178, 243, 245

Arhythmorhynchus longicollis
(Spiny-headed Worm), 190

Ascaridia galli (Roundworm),
183

^5cam (Roundworms), 180

Ascaris lumbricoides (Round-
worm), 44

Ascaroidea (Roundworms),
183

Asellus aquaticus, see Hog
Slater

Aspergillus fumigatus (Fungus),
243, Fig., p. 10

Assassin Bug (Rhodnius pro-
lixus, 20

Assassin Bugs (Reduviidae),
248

Atheta nidicola (Rove Beetle),

Atheta nigricornis (Rove

Beetle), 249
Atheta oloriphyla (Rove

Beetle), 249
Atheta trinotata (Rove Beetle),

249
Attagenus pellio (Beetle), 248
Aucheromyia sp., see Floor

Maggots
Auklet {Ptychorhamphus aleut-

icus), 90
Auks (Alcae), 130, 183, 195
Australian Black Swan {Chen-

opis atrata) , 1 94
Austromenopon (Feather Lice),

153

Avian Malaria {see also Plas-
modium), 2, 7, 33, 36, 164,
165,215

Avocet {Recurvirostra avosetta),
160, 173

Bacillus, see Bacteria

Bacillus anthracis (Bacterium),

236, 239
Bacteria, 29, 36, 1 20-1 21,

22, 235-239
Bacteriaceae (Bacteria). 237

Bairamlia fuscipes (Hymenop-

tera), 103
Balfouria monogama, 39
Bald Eagle {Haliaeetus leu-

cocephalus), 125
Barnacle Goose {Branta leu-

copsis), 1^-15
Barnacles (Cirripedia), 47
Barn-Owl {Tyto alba), 21,

184, 222, 225, 236, 251,

PL VI (23)
Barn-Swallow [Hirundo rust-

ica erythrogaster) , 247
Bat, 62, 97, 111,217
Bat Flea, 84, 94
Bay-winged Cow-bird [Mol-

othrus badius), 265
Bearded Tit {Panurus biarmi-

cus), no
Beaver, 62
Bed-bug (Cimex lectularius) ,

2, 53, 121, 247
Bee-eater [Merops apiaster),

12, 150
Bee-eaters {Merops sp., see

also Carmine Bee-eater), 1 2
Bees [and Wasps], 13, 26,

27,55
Beetles (Coleoptera), 2, 45,

51,52,246,248-250
Bilharziella palonica, see Duck

Blood-Fluke
Bird-bottle Fly, see Protocal-

liphora azurea
Birds of Prey, 14, 15, 24, 94,

183, 188, 190,249
Bittern {Botaurus stellaris),

152,. 237
Blackbird {Turdus merula),

85, 165, 169, 171, 181,

185, 189, 221, 222, 230,

240, PI. IV (15)
Black-flies (Simuliidae), 49,

169, 185, 211-212, 218-

220
Black-headed Gull {Larus

ridibundus), 15, 17, 206
Black-necked Grebe {Podi-

ceps nigricollis) , 1 5
Black-necked Stilt {Himan-

topus mexicanus) 194
Black-throated Diver {Col-

ymbus articus), 197
Black-winged Stilt {Himan-

topus himantopus), 194
Black Redstart {Phoenicurus

ochrurus), 1 12
Bladder Snail {Physa sp.), 18

Blennies {Blennius), 202
Blow-flies (Diptera), 243
Blue Tit {Parus coeruleus), 18,

25, HI, 169
Bluebottles (Calliphoridae),

211-212, 220-223, 55
Boa-constrictors, 232
Boreal Flea {Ceratophyllus

borealis), lio-lll, 87, 94
Borrelia anserinum (Spiro-

chaete), 232
Brambling {Fringilla monti-

fringilla), 169
Bream {Abramis brama), 195
Brent Goose {Branta bernicla),

12,46,253
Brook Trout {Salvelinus fon-

tinalis), 195
Bruelia (Feather Lice), 150
Buff"-backed Heron {Ardeola

ibis), 24.
Bugs (Hemiptera), 3, 7, 41,

48, 52, 120, 245, 247, PI.

XXXVI (259)
Bulbuls (Pycnonotidae), 12,

254
Bullfinch {Pyrrhula pyrrhula),

225, 237
Bumble-bee (Hymenoptera),

136, 293
Buntings {Emberiza), 165
Bustards (Otididae), 13
Butterfish {Pholis), 202
Butterfly, 43, 68, 70, 73, 87,

109, 114, 136, 220
Buzzard {Buteo), 14, 15, 173,

186, 189, 249

Calliphora (Flies), 221
Calliphoridae (Flies), 220
Camel, 171, 178
Campanulotes (Feather Lice),

154

Canary, 4, 36, 211

Canary-pox (Virus disease),
241

Capercaillie ( Tetrao urogal-
lus), 183

C(3/?z7/ana (Roundworms), 186

Capillaria annulata (Round-
worm), 186

Capillaria columbae (Round-
worm), 186

Capillaria contorta (Round-
worm), 186

Capraiella (Feather Lice), 150

Caprimulgiformes (Night-
jars), 150

286

FLEAS, FLUKES AND CUCKOOS

Carcinus maenas, see Shore
CraU-

Carduiceps (Feather Lice), 154

Carmine Bee-eater [Merops
nubicus), 13

Carnidae (Flies), 220-223

Camus hemapterus (Nest-fly),
7, 41, 222

Carrion-Crow (Corvus corone),
loi, 112, 127, 181, 184,
193. 195. 222, 249

Cat, 6, 76, 93, 94, 194, 253

Cat Flea (Ctenocephalides
felis), 76, 93

Catatropis vernicosum (Fluke),
202

Cattle, 7, 22, 24, 25, 215,
218, 232

Centipede, 181, 245

Centrorhynchus aluconis (Spiny-
headed worm), 189

Centrorhynchus teres (Spiny-
headed worm), 189

Ceratophyllidae (Fleas), 95

Ceratophyllus (Fleas), 70, 91,

94» 95. 99. 107
Ceratophyllus borealis, see

Boreal Flea
Ceratophyllus diffinis (Flea) ,101
Ceratophyllus farreni, see Far-

ren's House-Martin Flea
Ceratophyllus fringillae , see

House Sparrow Flea
Ceratophyllus gallinae, see Hen

Flea
Ceratophyllus garei, see Duck

Flea
Ceratophyllus himndinis, see

Common Hoiase-Martin

Flea
Ceratophyllus lunatus (Flea), 95
Ceratophyllus niger (Flea), 1 1 1
Ceratophyllus riparius, see

American Sand-Martin

Flea
Ceratophyllus rossittensis , see

Crow Flea
Ceratophyllus rusticus, see

Scarce House-Martin Flea
Ceratophyllus styx, see Sand-

Martin Flea
Ceratophyllus vagabunda, see

Vagabond Flea
Ceratopogonidae (Flies), 220
Cestoda, see Tapeworms
Cestodaria (Tapeworms),

194
Chaffinch (Fringilla coelebs).

148, 169, 171, 226, 230,
237, 250

Charadriiformes (Plovers,
Waders, Gulls, Auks, see
also Waders), 154-155,
130, 133. HO, 163

Cheese Mites (Tyroglyphi-
dae), 227, 228

Cheletidae (Mites), 28, 227

Chelifer cancroides (Pseudo-
scorpion), 248

Cheu-can [Pteroptochus rube-
cula), 92

Chicken Louse {Menacanthus
stramineus), 44, 125

Chiff'-chaff {Phylloscopus

colly bita), 260

Chilomastix gallinarurn (Pro-
tozoa), 173, Fig. 2e p. 162

Chough {Pyrrhocorax pyrrho-
corax), 89

Chough Flea, see Frontopsylla
frontalis and Frontopsylla
laetus

Ciconiiformes (Storks, Her-
ons and Bitterns), 152,
130, 141

Ciconiphilus (Feather Lice),

^52

Cimex columbarius, see Pigeon

Bed-bug
Cimex lectularius, see Bed-bug
Citellophilus (Fleas), 92
Citellus (Ground Squirrel), 92
Clam (Mollusc), 205
Clegs (Tabanidae), 11, 25,

171
Cliff Swallow [Petrochelidon

albifrons) , 14, 169
Cnemidocoptes gallinae (Mite),

226
Cnemidocoptes mutans (Mite),

226, Fig. p. 228
Coccidia (Protozoa), 161,

222
Coccus (Bacterium), 161, 235
Cochlosoma anatinis (Proto-
zoa), 173
Cockle (Mollusc), 205
Cockroach, 73, 184
Coleoptera, see Beetles
Collyriculum faba (Fluke), 39
Coloceras (Feather Lice), 154
Colpocephalum (Feather Lice),

135
Columbicola (Feather Lice),

123

Columbicola columbae, see Com-

mon Pigeon Louse
Columbiformes (Pigeons and

Doves), 154, 163, 226
Colymbiformes (Divers), 153
Colymbus (Divers), 195
Common Eider [Somateria

mollissima), 1 10
Common Gull {Larus canus),

17, 206
Common House-martin Flea
{Ceratophyllus hirundinis), 1 08,

Pis. XVn (98) and

xxxni (242)

68, 72, 85, 86, 92, 94, loi
Common Louse-fly (Ornith-

omyia avicularia), 213, PI.

IX (34) .
Common Pigeon Louse {Col-
umbicola columbae), 123
Common Periwinkle {Littor-

ina littorea), 31, 202, 204,

PI. XXVHI (179)
Common Rat Flea {NosopsyU

lus fasciatus) , 68-70, 72-75,

84
Common Sandpiper {Actitis

hypoleucos), 194
Common Tern {Sterna hir-

undo), 135, 233
Contracaecum (Roundworms),

183
Contracaecum spiculigerum

(Roundworm), 183
Coot {Fulica atra), 54, 156,

182, 184, 253, 266
Copepoda (Fish lice), 3, 23,

47, 54. 194. 195
Cormorant {Phalacrocorax

carbo), 133, 147, 153, 189,

254. PI. XXXIV (243)
Cormorants (Phalacrocora-

cidae), 121, 147, 153,

183, 196, 231
Corn-Crake {Crex crex), no,

205

Coraciiformes (Kingfishers
etc.), 150, 163

Corvus splendens (Crow), 164

Corynosoma (Spiny-headed
Worms), 189, Fig. 4 (196)

Corynosoma strumosum (Spiny-
headed Worm), 189

Corynosoma tunitae (Spiny-
headed Worm), 189

Corynosoma turbidum (Spiny-
headed Worm, Fig. 4

(196)
Cotugnia (Tapeworms), 197

INDEX OF POPULAR AND SCIENTIFIC NAMES

287

Cotylurus cornutas (Fluke), 206
Cows, 16, 17, 20, 21, 24, 173
Cow-birds {Molothrus), 10,

24, 265, 267, 268
Craspedonirmus ( Feather Lice) ,

153
Craspedorrhynchus (Feather

Lice), 140
Crataerina pallida, see Swift

Louse-fly
Crested Tit {Parns cristatus),

43, 112
Crocodile, 23, 232
Crocodile Bird (Pluvianus

aegyptius), 23
Crossbill (Loxia curvirostra) ,

172
Crotophagus ani, see Tick Bird
Crow Flea {Ceratophyllus

rossittensis) , 46, loi, iii,

Crows (Corvidae), loi, iii,
124, 184, 189, 221, 222,
226, 231, 238, 261, 264

Crustacea, 188, 190, 194,
195. 207

Cryptocotyle jejuna, see Red-
shank Fluke

Cryptocotyle lingua, see Her-
ring-gull Fluke

Ctenocephalides felis, see Cat
Flea

Ctenophthalmus agyrtes, see
Field-Mouse Flea

Cuckoo {Cuculus canorus), 5,
9> 10. 36,37, 38, no, 126,
135-136, 189, 225, 256-
268, PI. XXXVIII (265)

Cuckoo Head-louse (Cucu-
loecus latifrons), 126, 136,
156

Cuclotogaster (Feather Lice),
PI. XXIII (146)

Cuculiformes (Cuckoos), 151,
163

Cuculiphilus (Feather Lice),
136

Cuculoecus (Feather Lice),
126, 136

Cuculoecus latifrons, see Cuckoo
Head-louse

Culex fatigans (Gnat), 215

Culex pipiens, see House-gnat

Culicidae (gnats, mosqui-
toes), 214-218

Culicoides (Midges), 220

Culicoides biguttatus (Midge),
220

Culicoides fascipennis ( Midge) ,

220
Culicoides impunctatus (Midge),

220
Culicoides obsoletus (Midge),

PI. XXIX (210)
Cummingsiella (Feather Lice),

154

Curlew {Numenius arquata),
3, 42, 121, 129, 130, 183,
I94> 231

Curlew Quill Louse {Actorni-
thophilus patellatus), 121

Cyclophyllidea (Tape-

worms), 194

Cyclops serrulatus (Copepod),

195
Cyclops strenuus (Copepod),

195
Cyclops viridus (Copepod), 1 95
Cynomyia mortuorum (Fly), 251
Cypria ophthalmica (Ostracod)

195
Cytodites nudus (Mite), 226
Cytolichiidae (Mites), 226

Dace (Leuciscus leuciscus), 195
Dactylaria (Fungi), 243
Dactylella (Fungi), 243
Daphnia (Water Fleas), 184
Daphnia pulex (Water Flea),

184
Dasvpsyllus (Fleas), 90, 91,

95
Dasypsyllus gallinulae, see

Moorhen Flea
Davaineidae (Tapeworms),

197
Deer, 212, 230
Degeeriella (Feather Lice),

Demodicidae (Mites), 227
Dendrophylus punctatus

(Beetle), 250
Dendrophylus pygmaeus

(Beetle), 250
Dennyus (Feather Lice), 121,

125
Dennyus truncatus (Feather

Louse), 121, 125
Dermanyssidae (Mites), 224
Dermanyssus gallinae (Mite),

224
Dermanyssus hirundinis (Mite),

224
Dermanyssus passerinus (Mite),

224
Dermanyssus quintus^Miie) ,22^

Dermatobia hominis (Warble

Fly), 212
Dermestes lardarius (Beetle),

248
Dermestes murinus (Beetle), 248
Diaptomus gracilis (Copepod),

.195
Diaptomus vulgaris (Copepod),

.195

Dilepis undula (Tapeworm),
PI. XXVII (178)

Diphyllobothrium (Tape-

worms), 194

Diplomonadida (Protozoa),

173-175
Diplophallus polymorphus

(Tapeworm), 194
Diplostomum spathaceum

(Fluke), 206
Dipper {Cinclus cinclus), 114,

225
Diptera, see Flies
Diving Petrel (Pelicanoides

urinatrix), 91
Dogs, 12, 45, 98, 125, 223,

226
Domestic animals, see also

Mammals, 16, 21-23, 24

25.. 171, 173
Dominican Gull [Larus domi-

nicanus), 91
Dorcadia dorcadia, see Roe-
deer flea
Doves, see Columbiformes
Dragonfly {Libellula quadri-

maculata), 136, 204, 220,

Fig. p. 198
Drongos (Dicruridae) 25
Drosophila, see Small Fruit

Fly
Duck (Anatidae), 39, 41, 49,

85,94, ioi» I4i> 152, 169,

174, 189, 190, 195, 218,

238, 243, 251, 265
Duck Blood-fluke {Bilhar-

ziella palonica) , 205
Duck Flea {Ceratophyllus

garei), 81, 85, 87, 94, 97,

loi, no, 169
Duck Leech {Protoclepsis

tesselata), 208, Fig. p. 210
Dunlin {Caladris alpina), 189
Eagle, 14, 15, 190
Earthworm, 53, 176-178,

183, 184
Earwig, 245
Eastern Crow {Corvus brachyr-

hynchos), 193

288

FLEAS, FLUKES AND CUCKOOS

Echidnophaga gallinaceus , see

Hen Stick-tight Flea
Echidnophaga niyrmecobii, see

Marsupial Stick-tight Flea
Echinorhynchus pachyacanthiis

(Spiny-headed Worm) , 1 90
Echinostomatoidea (Flukes),

205
Eider Duck {Somateria mol-

lissima), 195, 197, 225
Eiders (Somateria), 30
Eidmanniella (Feather Lice),

153

Eimeria (Protozoa), 160, 163

Eimeria avium (Protozoan),
163, Fig. 2a p. 162

Eimeridae (Protozoa), 161-
164

Elephant, 41, 50, 78, 208

Empusa (Fungi), 243

Enicmus minutus (Beetle), 250

Enoplida (Worms), 186

Entamoeba (Protozoa), 174
Fig. 2i p. 162

Entamoeba lagopodis (Proto-
zoan), 174

Entoconcha mirabilis (Mollusc),

47
Entomophthoraceae (Fungi) ,

243
Epidermoptes bilobatus (Mite),

226
Esquimo Curlew {Numenius

borealis), 194
Eudynamis (Cuckoos), 261
Eulaelaps novus (Mite), 227
Eulaemobothrion (Feather

Lice). 155
Eureum (Feather Lice), 150
Eutrichomastix gallinarum

(Protozoan), Fig. 2f p. 162

Falcolipeurus (Feather Lice),

140
Falconiformes (Birds of

Prey), 140, 151, 163-164
Falcons {Falco), 15, 173, 222
Falculifer rostratus (Mite), 226
Fannia (Flies), 251
Farren's House-Martin Flea

[Ceraiophyllus farreni), 85,

108-109
Feather Lice (Mallophaga),

3> 7> 9> 28, 41, 43, 44, 45,

46, 52, 56-60, 69, 70, 71,

72, 75, 84, 118-157, 193,

Pis. I, XXI, xxn,

XXIII, XXIV (6, 130,

131, 146, 147)
Feather Mites (Analgesidae),

28, 42, 225, 226, PI.

XXXI (226)
Fieldfare [Turdus pilaris), 15
Field-mouse Flea (Ctenoph-

thalmus agyrtes) , 76
Filaria (Roundworms), 43,

98, 125, 172, 217, 219
Filicollis (Spiny - headed

Worms), 190
Filicollis anatis (Spiny-headed

Worm), 190
Fimbriaria fasciolaris (Tape-

vvorm), 195
Finch Louse-fly {Ornithomyia

fringillina) , 2 1 3-2 1 4
Finches (Fringillidae), 80,

85, 165, 222, 225, 226, 240
Fish,23, 32, 47, 78, 161, 178,

183, 187, 189, 194, 206,

208, 217, 233, 239, 254
Fish Crow {Corvus ossifraga),

.1937194
Fish lice, see Copepoda
Flamingoes, see Phoeni-

copteridae
Fleas, (Aphaniptera), 3, 41,

45> 5^ 52, 56-ii7» ^7i>
177, 217, 227, 228, 245,
248, 249, 251,252, Pis. V,
X, XI, XII, XIII-XVI,
XVII, XVIII, XIX,
XXXIII (22, 35, 50, 51,
66-67, 82-83, 98, 99, 114,
242) _
Flesh-flies (Sarcophaga) , 221
Flies (Diptera), i, 3, 7, 16,41,

45, 49, 51, 52, 163, 197,
211-223, 228, 245, 248,
251, 252, Pis. IX, XII,
XXIX, XXX,(34,5i, 210,
21 1

Floor Maggots {Aucheromyia
sp.), 44

Flukes (Trematoda), 35, 39,

42,45,48,145, 176-178,
192-208

Fly Larvae, 9, 28, 48, 49,

50, 5^ 247, 251
Flycatchers (Muscicapidae),

25, 247, 248, 250
Fonsecaonyssus sylvarum (Mite),

225
Formica rufa, see Wood Ant
Fowl or Chicken [Gallus

domesticus) , 1 1 1 , 121, 126-

127, 137, 156, 163, 168,

172, 173, 174, 179, 181,

183, 184, 186, 187, 195,
204, 218, 219, 220, 224,
226, 227, 231, 237, 238,
239, 241, 247, 263, 267

lowl cholera, 238

Fowl Leukaemia Virus, 241

Fowl Paralysis Virus, 241

Fowl Pest Virus, 241

Fowl relapsing fever, 232

Fowl Tick [Argas persicus) 232

Fowl-pox Virus, 31, 241

Fox, 15, 94

Franklin's Gull {Larus pipix-

can), 15
Fresh-water Shrimp (Gam-

marus pulex) , 184, 189, 195
Frigate Birds (Fregatidae),

254
Frog, 25, 42, 185, 189, 207,

208, 209, 216
Frontopsylla (Fleas), 95
Frontopsy Ha frontalis (Chough

Flea), 100
Frontopsylla laetus (Chough

Flea), 100
Fulicoffula (Feather Lice), 155
Fulmar Petrel [Fulmarus

glacialis), 17, 149, 153,

197, 231, 240
Fungus, 28, 128, 197, 217,

222, 251, 242-244

Gadwall (Anas strepera), 189

Galliformes (Game-birds)

129, 130, 156, 163, 183,

184, 197, 227
Game-birds, see Galliformes
Gammarus (Fresh-water

Shrimps), 184, 186, 195,

204
Gammarus pulex, see Fresh-
water Shrimp
Gannet {Sula bassana), 189,

226, 231, 254, 255
Gape-worm, see Syngamus

trachea
Garganey {Anas querquedula) ,

184, 195, 205
Gentoo Penguins {Pygosceles

taeniata), 13, 197
Giardia (Protozoa), 159, 173
Geese, 12, 85, loi, 163,

174. 183, 195, 205, 220
Gigantobilharzia (Flukes), 205
Giraffe, 22
Glaucous Gull {Larus hyper-

boreus), 197, 233

INDEX OF POPULAR AND SCIENTIFIC NAMES

289

Glossina morsitans, see Tsetse

Fly
Glossiphonidae (Leeches),

208
Gnathoncus (Beetles), 249
Gnathoncus buyssoni (Beetle),

250
Gnathoncus nidicola (Beetle),

250
Gnathoncus punctulatus (Beetle) ,

249. Fig- P-. 117
Gnats (Culicidae), see also

Mosquito, 7,185, 214-218,

220
Goat, 212
Goby {Gobius minutus), 32,

52, 201, 202, Pis. VII,

XXVIII (30, 179).
Godwit {Limosa lapponica) ,10^
Golden Eagle {Aquila chry-

saetus), 7, 152
Goldcrest {Regulus regulus),

18, 113
Golden-eye {Bucephala clan-

gula), 195, 206
Goldfinch {Carduelis cardu-

elu). 82, 237
Golden Oriole {Oriolus orio-

lus), 156
Goniocotes (Feather Lice), 128
Goniodes (Feather Lice), 128,

156
Goosander {Mergus mergan-
ser), 184
Grasshopper, 184, 185
Great-crested Grebe (Podi-

ceps cristatus), 197
Great Northern Diver (Col-

ymbus immer), 189
Great Shearwater {Puffinus

gravis), 13, 17
Great Skua {Stercorarius

skua), 254
Great Spotted Cuckoo {Cla~

mator glandarius), 258, 264
Great Spotted Woodpecker

{Dryobates major), 189, PI.

11(7).
Great Tit (Parus major), 18,

25, 165, 247, 249, 250,

PI. Ill (14)
Greater Black-backed Gull

(Larus marinus), 206, 254
Greater Yellowshank ( Tringa

melanoleucos) , 194
Grebes, see Podicipitiformes
Green-bottle Fly (Lucilia),

181, 221

Greenfinch {Chloris chloris),

224
Greenland Falcon {Falco

rusticola), 231
Green Sandpiper ( Tringa

ochropus), 225
Green Woodpecker (Picus

viridis), 151, 224
Gregarines (Protozoa), 103
Grey Phalarope (Phalaropus

fulicarius), 23
Grey Seal {Halichoerus gry-

phas), 189
Grouse {Lagopus scoticus), 3,

38, 163, 169, 174, 181,

230, 241

Grouse Louse-fly [Ornith-

omyia lagopodis), 213
Grouse Roundworm ( Tricho-

strongylus pergracilis) , 38,

181
Gruiformes (Coots and

Moorhens), 163
Gudgeon {Gobio Jluviatilis) ,

195
Guillemot {Uria aalge), 183,

195. 205, 225, 231, 255
Guillemot Tick [Ixodes uriae),

231, 232
Guinea-pig, 75

Gulls (Laridae, Larus sp. or
suborder Lari), see also
Sea-gull, 15, 17, 32, 45,
130, 143. i73> 190J I94»
195. 197, i99» 204, 205,
206, 224, 225, 240, 253,
254, 266

Gyrocelia (Tapeworms), 193

Haemaphysalis cinnabarina
(Tick), 231

Haemaphysalis leporis-palustris
(Tick), 231

Haematobia (Flies), 136

Haemogregarines (Proto-
zoa), 170

Haemophilus gallinarum (Bac-
terium), 239

Haemoproteidae (Protozoa),
170

Haemoproteus (Protozoa) , 167,
169, 170, 172, 214, Fig. 2c
p. 162

Haemosporidia (Protozoa),
164

Hair-follicle Mites (Demodi-
cidae), 227

Halipeurus (Feather Lice), 153

Halteridium, see Haemoproteus
Hang-nests (Ictcridae), 265
Hare, 98

Harpyrynchus (Mites), 227
Harvest Mites (Trombi-

diidae), 227
Hawks (Accipitridae), 6,

129, 135. 137. 148, 149.

151. 205, 222, 250
Hectopsylla psittaci, see Parrot

Stick-tight Flea
Hedge-Sparrow (Prunella

modularis), 221, 222, 225,

250, 252, 258, 263
Hedgehog, 69, 230
Helmet Fleas (Stephano-

circidae), 100
Helomyzidae (Flies), 251
Hemiptera, see Bugs
Hen Flea (Ceratophyllus gal-

linae), 46, 68, 69, 70, 72,

73, 81, 84, 86, 91, 93, 94,

97, loi, III, 249, Pis. X,

XI (35, 50)
Hen Stick-tight Flea (Echid-

nophaga gallinaceus) , 58, 62,

63, 68, 70, 74, 79, 84, 99
Heron (Ardea cinerea), 44
Heron Louse-Fly {Lynchia

albipennis), 214
Herons (Ardeidae), 159, 173,

184,225,233, 249
Herring-gull [Larus argenta-

tus), 17, 87, 197, 202, 206,

241
Herring-gull Fluke [Crypto-

cotyle lingua), 31, 32, 39,

206, Fig. 5 p. 203, Pis.

XXVII, XXVIII (178,

179)-

Heterakis (Roundworms), 1 72

Heterakis gallinae (Round-
worm), 183

Heterophyids (Flukes), 205

Hexamita (Protozoa), 173

Hippoboscidae, see Louse

files

Hippopotamus, 2

Hirudo medicinalis, see Medi-
cinal Leech

Hlster merdarius (Beetle),
100, 250

Histeridae (Beetles), 249

Histomonas meleagridis (Proto-
zoa), 172, 183

Histrichopsylla talpae, see Mole
Flea

Hobby {Falco subbuteo), 15

290

FLEAS, FLUKES AND CUCKOOS

Hofmannophila pseudospretella

(Moth), 251
Hog Slater {Asellus aquaticus),

190
Hohorstiella (Feather Lice),

154

Holotnenopon (Feather Lice),

Honey Buzzard {Pernis api-

vorus), 233
Honey-guides (Indicatori-

dae), 10, 268
Hooded Crow (Corvus cornix)^

Hoopoe {Upupa epops), 150
Hoplopsyllus (Fleas), 93
Hoplopsyllus glacialis lynx

(Flea), 92
Hornbills (Bucerotidae), 226
Hornets, 27
Horse, 7, 16, 76, 172, 208,

212
House-flies (Muscidae), 11,

55, 211-212, 220-223,

243

House-fly {Musca domestica),
181

House-gnat {Culex pipiens),
165, 172, 211, 215, 216
241,243, PI. XXX (211)

House-martin (Martula urb-
zVfl), 43, 61, 79,85,92, 171,
247, 248, 251, PI. XXXIX

(268)

House-martin Flea, see Com-
mon House-martin Flea

House-sparrow Flea [Cerato-
phyllus fringillae), 62, 94,

Houttuynia struthiocameli
(Tapeworm), 145, 194

Human Flea {Pulex irritans),
44, 70, 72, 73, 92, 94, 107

Human Louse {Pediculus hum-
anus), 139

Humming-birds (Trochili-
dae), 28

Hyalomma marginatum (Tick),
231

Hydracnid Mites, 217

Hydrobia, see Spire Shell

Hydrotaea (Flies), 251

Hymenolepidae (Tape-

worms), 195

Hymenolepis (Tapeworms),

i94» 195
Hymenolepis anatina (Tape-
worm), 195

Hymenolepis himantopodis

(Tapeworm), 194
Hymenolepis macracarthos

(Tapeworm), Fig. 4 p. 196
Hymenoptera (Bees, Ants

and Wasps), 26, 27, 55,

232, 245, 251
Hyphomycetales (Fungi) 243
Hypoderma bovis (Warble

Fly), 215

Incidifrons (Feather Lice), 1 55
Indian Hawk Cuckoo {Hier-

ococcyx varius), 263
Influenza Virus, 44
Insects, 18, 21, 27, 28, 34, 42,

43^ 64, 72, 195, 207, 240,

245, 246, 248, 249, 255
Ischnocera (Feather* Lice),

132, 139, 143, 148-156 PI.

xxn (131)

Isospora (Protozoa), 163,

164
Itch Mites (Sarcoptidae),

226
Ivory Gull (Pagophila eburnea),

13, 233
Ixodes (Ticks), 231
Ixodes brunneus (Tick), 231
Ixodes canisuga (Sand-martin

Tick), 231, 250
Ixodes caledonicus (Tick), 231
Ixodes passericola (Tick), 231
Ixodes ricinus, see Sheep Tick
Ixodes unicavatus, see Shag

Tick
Ixodes uriae, see Guillemot

Tick
Ixodidae (Ticks), 39, 229,

230
Ixodoidea, see Ticks

Jackal (Canis aureus), 190
Jackdaw (Corvus monedula),

11, 23, 27, 89, 115, 146,

171, 181, 189, 231, 245,

247, 250
Jack Snipe [Lymnocryptes

minimus), 195
Jay [Garrulus glandarius), 169,

171, 181, 226
Jelly-fish, 42, 53
Jigger [Tunga penetrans), 44,

Joubertia microphyllus (Mite),
226, PI. XXXI (226)

Jungle Fowl [Callus gallus),
69, 156

Kea, {Nestor notabilis) 18, 23
Kentish Plover {Leucopolius

alexandrinus) , 189
Kestrel [Falco tinnunculus) , 14,

181, 184
Kingfisher (Alcedo atthis), 14,

150, 190
Kingfishers (Alcedinidae),

see also Coraciiformes, 190
Kites (Alilvus), 14
Kittiwake (Rissa tridactyla),

97, 115, 206, 255
Kittiwake Flea {Mioctenop-

sylla arctica), 97
Koala Bear, 43
Kudu Antelope, 22
Kurodaia (Feather Lice), 151

Laelaptidae (Mites), 227
Laemobothriidae (Feather

Lice), 148
Laemobothrion (Feather Lice),

135, 148, 151
Lagopoecus (Feather Lice),

156
Laminosioptes cysticola (Mite),

226
Lampern [Petromyzon fluvi-

atilis), 195
Lapwing (Vanellus vanellus),

25> 230
Lark (Calandrella dukhunen-

sis), 164
Larks (Alauda), 165, 229, 230
Lathridiidae (Beetles), 250
Leeches (Hirudinea), 3, 7,

31, 41, 42, 46, 49, 50,

171, 176-178, 206, 207,

208-210
Legionary Ants (Dorylinae),

Leopard, 233

Leprosy (Bacillus), 98

Leucocytozoon [Vtoiozoz.) , 167,
169, 172, 217, Fig. 2b p.
162

Libellula quadrimaculata, see
Dragonfly

Ligula iniestinalis (Tape-
worm), 177, 195^

Limnaea (Pond Snails), 205,
206

Linnet [Carduelis cannabina),

171, 221, 252, 257
Lipeurus (Feather Lice), 156
Little Auk {Alle alle), 225
Little Owl {Athene noctua),

172, 181, 189,238

INDEX OF POPULAR AND SCIENTIFIC NAMES

291

Little Tern (Sterna albifrons),

I5» 155
Littorina littoreay see Common

Periwinkle
Lizard, 185
Long-eared Owl [Asio otus),

230
Long-tailed Duck [Clangula

hyemalis), 195, 208
Long-tailed Skua [Stercorarius

longicaudatus) , 254
Long-tailed Tit [Aegithalos

caudatus) , 14, 15
Louse, 7, 120
Louse-flies (Hippoboscidae),

52, 128, 136, 170, 211-

214, 252, Fig. p 157,
PI. IX, 34

Lucilia, see Green-bottle Fly
Lunaceps (Feather Lice), 154
Lung Mites (Gytolichiidae),

226
Lyctocoris campestris, see Antho-

corid Bug
Lynchia albipennis see Heron

Louse-fly
Lynx [Felis lynx), 190

Macronyssidae (Mites), 225
Maggots, 9

Magpie {Pica pica), 23, 24,

181, 220, 221, 264, 265

Malaria, see Avian malaria

Mallard {Anas platyrhyncha) ,

132, i73» i90> 195. 205,
206

Mammals, 42, 48, 50, 59,
76, 93, 186, 189, 194, 207,
208, 209, 212, 216, 217,
218, 219, 220, 227, 229,
230, 232, 236, 239, 242,
243, 249, 255

Man {Homo sapiens), 3, 16,
17, 20, 21, 33, 36, 44, 49,
54> 94> 98, 164, 170, 173,
174, 177, 180, 184, 186,
194, 205, 206, 207, 208,

215, 216, 226, 233, 236,
237, 240, 241, 242, 247,
248

anx Shearwater {Puffinus

puffinus), 143, 153, 197,

241, 243
Marabou Stork {Leptoptilos

crumeniferus), 39
Maritrema oocystai^\\ySs£) , 204
Marsh-Sandpiper ( Tringa

stagnatilis), 194
FFC -U

Marsupial Stick-tight Flea
{Echidnophaga myrmecobii),
69
Marsupials, 100
Marten, 95
Martins {Martula), 16, 17,

66, 67, 95, loi, 245, 250
Mastigophora (Flagellata),

160, 170-173
Meadow-Pipit {Anthus pra-

tensis), 221, 258, 289, 260
Medicinal Leech {Hirudo

medicinalis) , 209
Megninia strigis-otis (Mite),

225
Melophagus ovinus, see Sheep

Ked
Menacanthus (Feather Lice),

142, 149, 150, 156
Menacanthus stramineus

(Chicken Louse), 121
Menopon (Feather Lice), 156
Menoponidae (Feather Lice) ,

148
Meoneura (Nest FUes), 251
Meoneura lamellata (Nest Fly),

222
Meoneura neottiophila (Nest

Fly), 222
Merganser {Mergus serrator),

i95j 202, 206
Merlin {Falco columbarius) , 15
Meropoecus (Feather Lice), 1 50
Mice, I, 2, 30, 36, 80, 91,

208, 253
Michaelichus bassani (Mite),

226
Microfilariae (Larval

Roundworms), 185
Microglotta gentilis (Rove

Beetle), 249
Microglotta nidicola (Rove

Beetle), 249
Microglotta picipennis (Rove

Beetle), 249
Microglotta pulla (Rove

Beetle), 249
Microlichus avus (Mite), 226
Micro-parasites, 235-244
Microphallidae (Flukes), 204
Midges (Ceratopogonidae),

3, 7, 220, 243, PI. XXIX

(210)
Miller's Thumb {Cottus

gobio), 195
Mioctenopsylla (Fleas), 95
Alioctenopsylla arctica, see

Kittiwake Flea

Mites (Acarina), 3, 9, 18,
28, 36, 42, 45, 48, 50, 51,
52, 104, 128, 155, 195,
197, 217, 222, 224-234,
243. 245, 246, 248, 250,
252, Pis. V, XXXI (22,
226).

Mole, 12, 184

Mole Flea {Histrichopsylla
talpae), 61

Mollusc, 30, 45, 52, 195, 205,
207

Moniezia (Tapeworms), 197

Monilia (Fungi), 243

Monkeys, 26

Monopis ferruginella (Moth),

251

Monopis rusticella (Moth), 251

Monopsyllus anisus (Flea), 94
Monopsyllus sciurorum, see

Squirrel Flea
Moorhen {Gallinula chloro-

pus), 156, 168, 190
Moorhen Flea {Dasypsyllus

gallinulae), 84, 85, 86, 91,

92, 113

Mosquitoes (Culicidae), see
also Gnats, 3, 42, 46, 48.
49. 77. 136, 165, 167, 185,
208, 211-212, 214-218,

219, 241, 243
Moth Larvae, 251

Moths (Lepidoptera), 217,

220, 228, 245, 251
Motmots (Momotidae), 144
Mourning Dove {^enaidura

carolinensis) , 169-170
Mucor (Fungi) 243
A/w/c/zVo/fl (Feather Lice), 150
Mussel, see Mytelus, Unio,

Anodonta
Musca domestica, see House-fly
Muscidae, see House-flies
Mute Swan {Cygnus olor),

189, 194
Mycobacteriaceae (Bac-

teria), 236
Mycobacterium (Bacteria), 236
Myialgopsis trinotoni (Mite),

153
Mynahs, 24, 25
Myrsidea (Feather Lice), 149
Mytilus edulis (Marine Mus-
sel), 30, 205, Fig. p. 37.

Naubates (Feather Lice), PI.

XXIII (146)
Nematoda, see Roundworms

292

FLEAS, FLUKES AND CUCKOOS

Nematoparataenia (Tape-

worms), 194
Neopliilopterui (Feather Lice),

152
Neottiophilum (Flies), 251
Neottiophilum praeustum (Nest

Fly), 221
Nest Flics (Carnidae),2ll-

212, 220-223
Newts (Triton), 209, 217
Nightjar (Caprimulgus euro-

paeus), 150, 165, 225,

.256
Nightingales (Luscinia), 189,

I95> 221
Nosopsyllus fasciatus , see Com-
mon Rat Flea
Notocotylids (Flukes), 205
Nutcracker {Nucifraga cary-

ocatactes), 184

Oeciacus hirundinis, see Swal-
low Bug

Oestrus ovis, see Sheep Bot-
fly

Oidium (Fungi), 243

Onchocerca (Roundworms),
185, 219

Opisthorchioidea (Flukes),
202, 207

Opossum, 26

Oribata geniculatus (Mite), 246

Orneacus (Fleas), 95

Orneacus rothschildi, see Scot-
tish House-Martin Flea

Ornithobius (Feather Lice),

152, 153
Ornithomyia avicularia, see

Common Louse-fly
Ornithomyia fringillina, see

Finch Louse-fly
Ornithomyia lagopodis, see

Grouse Louse-fly
Ornithopsylla laetitiae, see

Shearwater Flea
Osprey [Pandion haliaetus),

14, 15, 207
Ostracods, 195
Ostrich {Struthio camelus),

142, I45> 194
Ostriches, see Struthioni-

formes
Oustaletia pegasus (Mite), 226
Oven-bird (Furnarius rufus),

247-248
Oviduct Fluke {Prosthogoni-

mus ovatus), 204
Owls (Strigidae), 31,94, 128,

157. 152, 169, 231, 239,
241, 246, 249, 250, 256

Ox-peckers (Buphagus), 21-
22, 23, 24

Oxylipeurus (Feather Lice),
156

Oxyspirura mansoni (Roun-
worm), 184

Oxyspirura sygmoidea (Round-
worm), 184

Oyster-catcher [Haematopus
ostralegus), 129, 189, 204

Paralges pachycnemis (Mite),

145
Parrakeet {Eupsittula cani-

cularis), 251
Parrakeet (Platycercus uni-

color), gi
Parrakeet [Psephotus chrysop-

terygius), 251
Parrot Stick-tight Flea {Hec-

topsylla psittaci), 62, 63, 93
Parrots (Psittacidae), 14, 93,

128, 1240
Partridge {Perdix perdix), 85,

94, 102, 129, 181, 226,

241
Passer domesticus indicus (Spar-
row), 194
Passeriformes (Passerines),

1445 149, 150, 165, 188,

189, 214, 224, 227, 257,

261, 263
Pasteurella aviseptica (Bac-
terium), 239
Pasteurella pestis (Bacterium),

238
Peacock {Pavo cristatus), 186
Pecten, see Scallop
Pectinopygus (Feather Lice),

153, PI. XXII (131)
Pediculus humanus, see Human

Louse
Pelecaniformes (Pelicans and

Cormorants), 133, 153,

Pelicans (Pelicanidae), 3,

I33> H7>2o8, 215
Penenirmus (Feather Lice),

i49>. 150
Penguins (Spheniscidae), 91,

100
Penicillium (Fungi), 243, 244
Penicillium notatum (Fungus),

244
Pentastomida, see Tongue-
worms

Perch {Percafluvial'lis), 195
Peregrine Falcon {Falco pere-

grinus), 184
Perineus (Feather Lice), 153
Petrels (Oceanites), 13, 143
Phalacrocorax nigrogularis

(Cormorant), 125
Phaonia (Flies), 251
Pheasant (Phasianus colchi-

c«j), 156, 226,237,240,241
Philonthus (Rove Beetles), 249
Philonthus fuscus (Rove

Beetle), 249
Philopterus (Feather Lice),

133, 144, 149
Phoenicopteridae (Flamin-
goes), 59, 133, 141, 142,

146, 194
Phoridae (Flies), 251
Physa (Bladder Snails), 18
Piagetiella (Pouch-Lice), 121
Piciformes, see also Wood-
peckers, 150, 163
Pied Flycatcher {Muscicapa

hypoleuca), 258
Pied Wagtail {Motacilla alba),

258 PI. XXXVIII (265)
Pig, 16,44, 185
Pigeon (Domestic), 169, 173,

186, 197, 222, 224, 225,

227, 229, 231, 237, 240,

241, 248
Pigeon Bug {Cimex colum-

barius), 247
Pigeon Louse-fly [Pseudo-

lynchia maura), 214
Pigeon-pox (Virus disease),

36, 241
Pigeon Tick (Argas reflexus),

231, 232
Pike (Esocidae), 195
Pink-footed Goose {Anser

brachyrhynchus) , 202
Pintail {Anas acuta), iio, 173
Pipits (Anthus), 207, 259
Piroplasma (Protozoa), 170
Plagiorchioidea (Flukes),

189, 204
Plagiorhynchus crassicollis

(Spiny - headed Worm),

189
Plague bacillus (Pasteurella

pestis), I, 103, 238
Planorbis (Molluscs), 205
Plantain-eaters (Musopha-

gidae), 142
Plasmodidae (Malaria para-
sites), 164

INDEX OF POPULAR AND SCIENTIFIC NAMES

293

Plasmodium (Malaria para-
sites— see also Avian mal-
aria), 2, 7, 34, 164-170,
172, 241

Plasmodium falciparum (Mal-
aria parasite) Fig. 3, p. 166

Plasmodium gallinaceum (Mal-
aria Parasite), 168

Plasmodium relictum { = P-
praecox), 165, 170, 217

Platypsyllus castoris (Beetle),
62

Pleochaetis (Fleas), 91

Plovers, 18, 204, 205, 225,
228, 263

Pochard [Aethyia ferina),
184, 195

Podicipitiformes (Grebes),
153. 183, 193, 195, 206

Polyctenidae (Bugs), 188

Polymorphidae, 310

Polymorphus boschadis (Spiny-
headed worms), 189, 190

Pomatorhine Skua {Ster-
corarius pomarinus), 254

Porpoise, 13

Porrocaecum (Roundworms),
183

Porrocaecum depressum (Round-
worm), 184

Powan [Coregonus lavaretus),

195
Prairie Falcon {Falco mexi-

canus), 14

Procellariiformes (Petrels),
130

Proctophyllodes glandarius
(Mite), 226

Prognesubis, see Purple Mar-
tin

Progynotaenia (Tapeworms),

193
Prosthogonimus oiatus, see

Oviduct Fluke
Prosthorhynchus transversus

(Spiny - headed Worm),

189
Protalges attenuatus (Mite), 225
Protocalliphora azurea (Bird-
bottle Fly), 7, 221, Fig. p. 5
Protocalliphora (Flies), 221,

251
Protoclepsis tesselata, ses Duck

Leech

Protomonadida (Protozoa),

171-173
Protophyllodes glandarius
(Mite), 226

Protozoa, 3, 7, 9, 29, 36, 39,

41, 42, 52, 159-175, 197,

217, 222
Psephotus chrysopterygius , see

Parrakeet
Pseudolynchia canariensis, see

Pigeon Louse-fly
Pseudomenopon (Feather Lice)
Pseudophyllidea (Tapeworms),

i94> 195
Pseudo-scorpions, 18, 248,

Psittacosis virus, 240
Ptarmigan (Lagopus), 15, 87
Pterolichus ardea (Mite), 225
Pterolichus bicaudatus (Mite),

145
Pterolichus cucidi (Mite), 225
Pterolichus obtusus (Mite), 226
Ptilonyssus nudus (Mite), 227
Puffin [Fratercula arctica), 90,

92, 94, 116, 231, 255
Pulex irritans, see Human Flea
Pulicidae (Fleas), 92, 95, 107
Purple (Mollusc), 205
Purple Grackle {Quiscalus

quiscula), 127
Purple Martin {Progne subis),

247
Purple Sandpiper (Caladris

maritima), 181, 190, 225
Pygiopsyllidae (Fleas), 91
Pythons, 232

Quadraceps (Feather Lice),
154, PI. XXIII (146)

Quail {Coturnix coturnix), 237,
241

Quill Louse, see Curlew
Quill Louse

Rabbit, 54, 92, 98, 230

Rabbit Flea [Spilopsyllus cun-
iculi), 63, 90, 92, 93, 94, 95
Pis. X, XI (35, 50)

Raillietina anatina (Tape-
worm), 197

Rainbow Trout {Salmo iri-
deus), 206

Rallicola (Feather Lice), 155

Ralliformes (Rails), 155-
156

Rat Flea, see Common Rat
Flea

Rats, 6. 45, 75, 79, 91, 94,

i7i» 179
Raven {Corvus corax), 231

Razorbill {Alca torda), 195
Red-backed Shrike {Lanius

collurio), 258, 259
Red-breasted Goose (Branta

rujicollis), 14
Red-breasted Merganser

[Mergus serrator), 110
Red deer, 230
Red Mite of Poultry, 172,

224, 238
Red-necked Phalarope {Pha-

laropus lobatus), 15
Redpoll (Carduelis Jlammea),

12
Redshank (Tringa totanus),

199, 202
Redshank Fluke (Cryptoco-

tyle jejuna), 199, 201, 202
Redstart {Phoenicurus phoeni-

curus), 221, 258, 259, 260
Red-throated Diver {Colym-

bus stellatus), 197
Reduviidae, see Assassin Bugs
Redwing {Turdus musicus),

230
Red-winged Crested Cuckoo

{Clamator coromandus), 263
Reed-warbler {Acrocephalus

scirpaceus), 37, 258
Reighardia sternae (Tongue-
worm), 233, Fig. 4, 196
Remora, see Sucking-fish
Reptiles, 161, 194, 232
Rhabditida (Worms), 180
Rhea {Rhea americana), 142
Rhea [Pterocnemia pennata),

139, 194
Rhinoceros, 21
Rhinonyssus neglectus (Mite),

225
Rhodnius prolixus, see Assassin

Bug
Rhynonirmus (Feather Lice),

154
Rhizopoda (Protozoa), 160,

173-174
Ricinidae (Feather Lice),

148
Ricinus CFeather Lice), 148,

149, PI. XXIII (146)
Ricinus rubeculae (Feather

Louse), 126
Ringed Plover {Charadrius

hiaticula), 189
Roach {Leuciscus rutilis), 195
Robin {Erithacus rubecula), 6,

12, 17, 73, 126, 148, 149,

189, 258, 259, PI. IV (15)

294

FLEAS, FLUKES AND CUCKOOS

Rock-dove (Columba livia),

i54> 231
Rock-dove Flea {Ceratophyl-

lus columbae), 62, 84, 100,

110
Rockling {Onos spp.), 202
Rock-thrush {Monticola saxa-

tilis), 190
Roe deer, 49
Roe-deer Flea {Dorcadia dor-

cadia), 49
Ko\\tr{Coracias garrulus), 150
Rook {Corvus frugilegiis), 17,

23, 26, 31, 85, 147, 149,

171,181,194,230,236,252
Rose-coloured Pastor {Pastor

roseus), 231
Roundworms {Nematoda) , 3,

40> 41. 43. 54> 99> 125,
176-187, 188, 189, 243,

245

Rous sarcoma virus, 241

Rove Beetles {Staphylinidae) ,
5, 28, 50, 51, loi, 249

Ruby-throated Humming-
bird {Archilochus colubris),
28

Ruffed Grouse {Bonasa um-
bellus), 229, 231

Sacculina (Crustacean), 47,

53. 130
Saemundssonia (Feather Lice),

153, 154, PL XXI (130)
Salmon (Salmo salar), 195
Salmonella (Bacteria), 98, 237
Salmonella pullorum (Bacter-
ium), 237
Sanderling {Crocethia alba),

189, 225
Sandhopper (Amphipod),

204
Sand-maitin [Riparia riparia),

45, 72, 80, 86, 227, 231,

249, 250, 251, Pis. XXVI,

XXXV (163, 258)
Sand-martin Flea {Cerato-

phyllus Styx), 62, 78, 80,

86, 97, loi, 113
Sand-martin Tick, see Ixodes

canisuga
Sandwich Tein {Sterna sand-

vicensis), 155
Sarcocystis (Fungi), 243
Sarcophaga, see Flesh-flies
Sarcoptidae, see Itch Mites
Sarcosporidia (Fungi), 243
Scallop (Molluscs), 290

Scarce House-martin Flea
{Ceratophyllus rusticus), 94

Scaup {Ayihya marila), 173,
189, 190, 206

Scenopinns fenestralis , see Win-
dow Fly

Schistocephalus (Tapeworms),

195
Schistosoma tidae (Flukes), 206

Schistosomes (Flukes), 205

Schistotaenia (Tapeworms),

193
Scoters {Alelanitta) , 30, 195,

206
Scottish House-martin Flea

{Orneacus rothschildi), 92,

104, IO8-IIO
Screaming Cow-bird {Molo-

thrus rufo-axillaris), 265
Sea Cucumbers (Holo-

thuria), 47
Sea-gulls, see Gulls
Seals, 19, 188, 194
Sedge-warbler {Acrocephalus

schoenoboenus) , 258
Shag {Phalacrocorax aristo-

ielis), 57 y 189, 195, 231
Shag Tick {Ixodes unicavatus),

231
Sharks (Carchariidae), 11,

Shearwater Flea {Ornithop-
sylla laetitiae), 63, 92, 93,
96, 97, 107, 115, Pis. XI,

XXXIII (50, 242)
Shearwaters {Puffinus), 90,

92, 94» I53> 241, PI.

XXXIV (243)
Sheath-bill {Chionis alba), 197
Sheath-bills (Chioidae), 13
Sheep, 16, 21, 23, 54, 78,

171, 212, 232
Sheep bot-fly {Oestrus ovis),

212
Sheep Ked {Melophagus

ovinus), 21, 43, 171, 213,

PI. IX (34)
Sheep Tick {Ixodes ricinus),

230, PI. XXXII (227)
Sheld-duck ( Tadorna tad-

orna), 90, 183, 189, 202
Shore Crab {Carcinus maenas),

204, Fig. p. 187
Short-eared Owl {Asio flam-

meus), 19, 184, 225
Shoveler {Spatula clypeata),

173
Shrew, 184

Shrikes (Laniidac), 160
Shrikes (Z,ar»'wj), 1 65, 173, 184
Simuliidae, see Black-flies
Simulium aureum (Black-fly),

219
Simulium latipes (Black-fly),

219
Simulium venustum (Black-fly),

218, 219
Siskin {Carduelis spinus), 237
Skuas {Stercorarius), 10, 143,

183, 205, 253-255
Sky-lark {Alauda arvensis),

221
Slender-billed Weaver {Tet-

eropis pelzelni), 14
Small Fruit Fly {Drosophila) ,

52
Small Golden Cuckoo {Lam-

promorpha caprius), 257
Smew {Mergus albellus), 206
Snails {see also Mollusc), 18,

19.35. 178, 197. 202, 204,

205, 206
Snake, 53, 216, 232
Snipe {Capella gallinago) , 129,

197. 238
Snow-shoe Hare, 229, 231
Song-thrush ( Turdus erice-

torum), 85, 165, 189, 227
South American Duck {Het-

eronetta atricapilla) , 266
Sparrow {Passer domes ticus),

17, 27, 39, 85, 93, 137,

170, 205, 221, 225, 226,

231. 235, 237, 238, 241,

244, 248, 249, 250, 265
Sparrow-hawk {Accipiter

nisus), 15, 85, 237, 256
Spider, 49, 245
Spilopsyllus cuniculi, see Rabbit '

Flea
Spiny-headed Worms (Acan-

thocephala), 186, 178,

188-191, 233
Spire Shell {Hydrobia ulvae),

199, 200, 202, 204, 205
Spirillum (Bacteria), 235
Spirochaetes (Bacteria), 31,

36, 238
Spiruroids (Worms), 185
Spoonbill {Platalea leucoro-

dia), 152
Sporozoa (Protozoa), 160-

170
Springtails, 181, 245
Squirrels, 14, 91, 94, 170,

230

INDEX OF POPULAR AND SCIENTIFIC NAMES

295

Squirrel Flea {Monopsyllus
sciurorum), 91, 94, PI. XIII
(66)

Stable-fly {Stomoxys calat-
rans), 221

Staphylinidae, see Rove
Beetles

Staphylococcus (Bacteria),

239, 244

Starfish, 11, 12, 47, 52

Starling {Sturnus vulgaris), 24,
25, 28, 85, 127, 136, 169,
181, 189, 197, 222, 237,
247, 251, 261, 265, PI.
VIII (31)

Starlings (Sturnidae), 21, 22,

23» i33» 235
Stenepteryx hirundinis , see

Swallow Louse-fly
Sternostomum caledonicum

(Mite), 225
Sternostomum waterstoni

(Mite), 225
Stickleback, 3 spined [Gas-

terosteus aculeatus), 195
Stoat, 6, 94, 95, 230
Stock-dove {Columba oenas),

17, 154, 246, 247, 265
Stomoxys calcitrans, see Stable-

Stone Curlew [Burhinus oedic-

nemus), 231
Storm-petrel {Hydrobates pel-

agicus), 153
Streptococcus (Bacteria), 239
Streptomyces griseus (Fungus),

244
Strigeoidea (Flukes), 206
Strigiformes (Owls), 151,

163
Strigiphilus (Feather Lice),

Strongylina CWorms), 180

Strong "loides avium (Round-
worm), 182

Struthiolipeurus (Feather

Lice), 142, 145

Struthioniformes (Ostriches),

13. 139, 142, i45» 1495,194
Sturnidoecus (Feather Lice),

149
Sucking-fish (Remoras), 11,

18
Sucking Louse (Anoplura),

121, 125, 138, 139
Sun-fish 12
Swallow (Hirundo ntstica), 12,

27, 43> 171

Swallow Bug (Oectacus hirun-
dinis), 2, 247

Swallow Louse-fly (Stenep-
teryx hirundinis) , 213, PI. IX

(34)
Swallow Red Mite (Der-

manyssus hirundinis), 224

Swallows {Hirundo), 16, 17,

49>85, 165, 169, 193, 207,

213, 217, 222, 225, 248,

251
Swallows and Martins (Hir-

undinidae), 79, 184, 215,

221, 247, 248, 251, 252,

265

Swans (Cygnus), 153, 195,
249, PI. XX (115)

Swift (Apus apus), 94, 213

Swift Louse-fly (Crataerina
pallida), 213

Swifts (Apus sp., see also
Apodiformes) , 16, 217

Swifts (Apodidae, see also
Apodiformes), 194

Sword-fish, 12

Syngamus merulae (Gape-
worm), 181

Syngamus trachea (Gape-
worm), 39, 180, PI.
XXVII (178)

Syringobia (Mites), 225

Syringophylus (Mites), 227

Tabanidae (Flies), 11, 16

Tapeworms (Cestoda), 2, 7,
31, 39, 40, 43, 45, 47, 52,
58, 98, 125, 176-178,
179, 188, 191-197, 222

Tatria (Tapeworms), 183,
184, 189, 193

Teal [Anas crecca), 195, 205,
208, 237

Termites, 13, 26

Terns (Sterna), 15, 194, 195,
197. 255, 263

Tetrabothrius (Tapeworms),

197

Tetrabothrius cylindraceus
(Tapeworm), 197

Tetrabothrius erostris (Tape-
worm), 197

Tetrabothrius macrocephalus
(Tapeworm), 197

Tetrameres (Roundworms),
179, 184

Tetrameres fissipinus (Round-
worm), 184

Thecarthra (Mites), 225

Theobaldia annulata (Mos-
quito), 165

Thrushes (Turdidae), 28, 80,
165, 169, 171, 172, i8r,
185, 190, 197, 221, 226,
227, 241, 250, 254

Tick Birds (see also Ani), 24,
25, 266

Ticks (Ixodoidea), 3, 7. 22,
32, 38, 40, 41, 42, 45, 46,
48, 208, 228, 229-232,
238, 245, Pis. XII,
XXXII (51, 227)

Tinamiformes ( Tinamous) ,
142, 147

Tinea lapella (Clothes Moth),
250^ Fig. p. 19

Tinea pellionella (Clothes
Moth), 250

Tits (Paridae), 18, 25, 195,
221, 222, 226, 249

Tongue-worms (Pentasto-
mida), 3. 232-234

Top-shell (Mollusc), 205

Tortoise, 171

Toxoplasma (Protozoa), 170

Trabeculus (Feather Lice),

153
Tree-creepers (Certhia), 195,

221

Trematoda, see Flukes

Treponema (Spirochaetes),
238

Treponema anserinum (Spiro-
chaete), 238

Trichinelle (VVorms),

Trichinella spiralis (Tape-
worm), 186

Trichobilharzia (Flukes), 205

Trichomonadidae (Proto-
zoa), 172

Trichomonas (Protozoa), 173

Trichomonas columbae (Pro-
tozoa), 173

Trichomonas eberthi (Proto-
zoa), Fig. 2d p. 162

Trichomonas foetus (Protozoa),

^73

Trichomonas gallinae (Proto-
zoa), 173

Trichomonas gallinarum (Pro-
tozoa), 173

Trichosomoides (Round-
worms), 179

Trichostrongylus pergracilis, see
Grouse Roundworm

Trichurata (Roundworms)
186

296

FLEAS, FLUKES AND CUCKOOS

Trinolon (Feather Lice), 128,
141, 152, 153, PI. XXII

(13O

Triton, see Newts

Trombidiidae, see Harvest
Mites

Tropical Rat Flea (Xenop-
sylla cheopis), 70, 72, 74,
74, 98, 107

Trouessartia minutipes (Mite),
226

Trox scaler (Beetle), 246, 250

Trox scabulosa (Beetle), 250

Trypanosoma equiperdum (Pro-
tozoa), 172

Trypanosoma fringillinarum
(Protozoa), 171

Trypanosoma gallinarum (Pro-
tozoa), Fig. p. 175

Trypanosoma lewisi (Proto-
zoa), 172

Trypanosoma loxiae (Protozoa) ,
172

Trypanosoma noctuae (Proto-
zoa), 172

Trypanosomes (Protozoa), 3,

36, 42, 54. 98, 1 71-173.

222, PI. XXV (1 62)
Tsetse Fly {Glcssina morsitans),

172, 212, 220
Tuberculosis (Disease caused

by A fy CO bacterium), 21
Tufted Duck (Aythya fuli-

gula), 15, 205, 253 _
Tunga penetrans, see Jigger
Turkey (Domestic), 164, 169,

172, i8r, 212, 218, 226
Turnstone {Arenaria inter-

pres), 15, 204
Turtle-dove {Streptopelia tur-

tur), 197
Tyroglyphidae, see Cheese

Mites

Unio (Freshwater Mussel), 30

Upupicola (Feather Lice), 150
Uria (Guillemots), 195

Vagabond Flea {Ceratophyl-
lus vagabunda), 87, 89, 115

Vibrio (Bacteria), 235

Vibrio metchnikovi (Bacter-
ium), 239

Virus, 36, 240-241

Vole, 69

Vulture, 14

Waders (Charadrii) 85, 129,

130, 189, 190, 193, 194,

199, 225, 266
Wagtails {Motacilla), 190,

207, 221, 259
Warble Flies {Dermatobia

hominis and Hypoderma

bovis), 212, 215
Warblers (Sylviidae), 80,

85, 165,214,221,222, 260
Wasps, 1 3, 26, 68, 97, 2 1 7, 248
Wryneck {Jynx torquilla), 1 10
Water Flea, see Daphnia pulex
Waxwing {Bombycilla gar-

rula), 12
Weasel, 94
Weavers (Ploceidae), 10, 14,

15. 24, 257, 265, 266, 268
Weddell Seals, 13
Weevils (Beetles), 185
Whale, II, 13, 23, 51, 188,

197
Wheatear {Oenanthe oen-

anthe), 258
Whelk (Mollusc), 47, 205
Whinchat {ScLxicola rubetra),

230, 258
Whiskered Tern {Chlidonias

hybrida), 15
White Stork (Ciconia ciconia),

152
White-tailed Eagle {Haliae-

tus albicilla), 14

Whitethroat {Sylvia com-
munis), 252
White Wagtail {Motacilla

alba), 14, 15, 165
Wigeon {Anas penelope), 12,

195, 206, 208, 253
Willow-tit {Parus atricapil-

lus), 113
Window Fly {Scenopinus fen-

estralis), 250
Wood Ant {Formica rufa), 14
Woodcock {Scolopax rusti-

cola), 126, 195
Wood Louse {Armadillium

vulgare), 184, 245
Woodpeckers (Picidae), 14,

142, 150, 184, 222, 265
Wood-pigeon {Columba pal-

umbus), 15, 17, 154, 169,

235, 236, 243, 245, 246
Wood-warbler {Phylloscopus

sibilatrix), 260
Worms, 3, 7, 9, II, 21, 30,

34. 35. 42, 48, 52, 176-
210, Pis. XXVII,
XXVIII (178, 179)

Wrasse {Labrus), 202

Wren {Troglodytes troglodytes),
14. 27

Xenopsylla (Fleas), 90
Xenopsylla astia (Flea), 75
Xenopsylla cheopis, see Tropi-
cal Rat Flea

Yellow Wagtail {Motacilla

flava), 25
Yellow-backed Oriole {Caci-

cus cela), 26
Yellow-billed cuckoo {Coc-

cyzus americanus) 266
Yellow-hammer {Emberiza

citrine I la), 171
Yellowshank {Tringa Jla-

vipes, see also Greater

Yellowshank), 194

INDEX OF POPULAR AND SCIENTIFIC NAMES

297

GENERAL INDEX

Abdomen, fleas, 64
Abortion, 173
Abscesses, 93

Abstinence, 73, 75, 97, 209
Acanthella, 189
Acid-fast bacteria, 236
Activity of flea and louse, 58
Adaptation, 4, 43-46 :
to brood-parasitism, 260;
to climatic conditions, 70;
confused views on, 1 79 ; to
clinging to feathers, 132;
of cuckoo's egg, 262; to
ecological niches, 131, 139;
of ectoparasites, 44; of
follicle-mites, 227; to hab-
its of host, 45, 46; of Icie,
126, 129; of mouth parts,
73» 139; mutual, 35; of
parasites, 35, 43, 69; to
pH, 192; of Protozoa,
159; to sedentary habit,

93
Adhesive discs, 1 1
Afterbirth, 13
Air-sacs, 3, 8, 207, 226, 232,

243

Alimentary canal, 3, 192

Ambulatory processes, 53

Ancestors, fleas', 63, 93, 118

Ant-birds, 254

Antennae :

fleas, 62, 64; lice, 122,
140; modified, 57, 64

Ant-hills, 14

Antibiotics, 243

Anting :

active, 127; functions of,
128; origin of, 127; pas-
sive, 127; soldiers', 127

Appetite, 72, 74

Asexual :

generations, 54; reproduc-
tion, 39, 41, 160, 173, 176,
200

Association :

nesting, 16, 23, 26; origin
of, 26; predator and prey,

137

Balance, host and parasite, 35
Bams, 16, 21
Bathing, 126
Beauty, 3, 198

Main Sections are in heav^ type

Behaviour, 18, 28, 36 :
mosquitoes, 215; sym-
biotic, 24

Bible quoted, i, 11, 15, 19,
33» 4i> 72, 158, 190, i93>
235> 256

Bile-duct, 3

Black Death, i

Blackhead, 172, 183

Blindness, 43 :

birds', 232; fishes', 207

Blinking, 33, 37

Blood, 3 :

clotting, 42, 74, 182, 209;
composition, 137; depend-
ence on, 46, 48; food of
fleas, 73; food of leeches,
31, 41, 209; food office,
121; food of mites, ticks,
225, 230; food of worms,
182, 198; quantity im-
bibed, 74; rat flea's, 72;
stimulus of, 68, 112, 216

Blood-letting, 210

Body-fluids, 44, 48

Bone-marrow, 171

Book-lice, 138

Bottles, milk, 18

Bracts, 217

Brain, flea's, 64

Bristles :

flea's, 78; -formula, 81;
reduced, 96

Bronchi, 3

Brood-parasitism, 9, 36, 38,
256 268 :

characteristics of, 267;
lice in, 137; origin of, 265;
rare, 265; specialisation
in, 268

Bubonic plague, i, 70, 98,
238

Budding of larvae, 39, 1 76,
182

Bush fires, 13, 25

Butter, 236

Canal, gynaecophorus, 39

Cannibalism, 121

Carriers, see Vectors

Carton nests, 14

Castration, parasitic, 31, 35,

103
Caterpillars as food, 256
Cathedrals, 84

Cave-dwelling, 42, 97, 109

Cercaria, 32, 42, 200-207

Chance, 38

Chitin, 62

Cigar-butts, 127

Classification, 104-108: ar-
bitrary, 10, 105 ; of
bacteria, 236; of cestodes,
194; of fleas, 62, 107; of
Ischnocera, 139; of lice,
129, 148; objects, in
science, 105; of parasites,

io> 59
Claws, 41, 78, 121
Clepto-parasitism, 10, 25,

253-255 :

frigate bird's, 253 ; cock-
erel's, 253; skua's, 10,254;
thrush's, 254; incipient,

253
Climbing, fleas', 78; lice,

122

Clotting of blood, 42, 74,
182

Cocoons, 72

Colds, 235

Collection, fleas, 61; lice,
147

Colour :

cuckoos' eggs, 259, 262;
fleas', 62; fleas' eggs', 70;
leeches' blood, 209; lice,
126; worms, 184, 198,

Combs, 52, 62; lost, 96

Commensalism, 4, II-19 :
ants', 14, 51; arthropods,
19; bacterial, 239; birds',
12,19; dangers of, 49 ; de-
fined, 11; fish's, 12; fish-
ermen and, 16; flies', 11;
fungal, 242; incipient, 15;
insects, 19; nidicoles, 245-
252; psychological ele-
ment, 16; rove beetles,
50; termites, 51

Communities, 109

Competition, 137 :

inter-specific, 35, 52, 128,
intra-specific, 35; spatial,

Conchiolin, 31
Convergence, 96
Coprophagy, 13, 28, 50
Copulation :

•298

FLEAS, FLUKES AND CUCKOOS

blackflies, 49, 218; Coc-
cidia, 161; cuckoo's, 257;
fleas', 64, 65, 68, 80, 184;
flukes', 40; horse's, 172;
leeches', 209; mites' 225;
mosquitoes', 215; tape-
worm's, 191; ticks', 230

Corpses eaten, 50, 51

Corpuscles, 3

Correlation, 129

Coryza, 239

Courtship, 252

Cow pox, 241

Cowsheds, 16, 71

Crop, 3 :

contents examined, 22,
25; of louse, 120, 121 ;
nematodes in, 183, 184;
protozoa in, 173

Cuckold, 262

Cuticle, 179

Cyst :

flukes', 39, 204; intestinal,
45; protozoal, 42, 160;
tongue-worm', 233

Cysticercus, 192

Cystogenous glands, 204

Cytostome, 160, 171

Death :

of host, 31-37, 57, 97,
104, 136, 163, 181, 186,
221, 225, 236; of male
flea, 68; of parasite, 38,104

De-leeching, 23

De-lousing:

of birds, 28, 232 ; of cattle,
24; of fish, 23; of mam-
mals, 22; of whales, 23

Dengue, 217

Dependence:

dangers of, 46; degrees
of, 9; parasites and, 54;
symbiotic, 20

Dermatitis, 228

Descent, fleas", 63

Development, direct, 233;
mites', 225; parasites' 48

Dew, 49

Diet, 6, 193, 256

Differences, specific, 140

Digestion, lice, 121

Digestive organs, flea's, 64

Diplostomulum, 207

Disease:

carried by fleas, 98-99;
carried by flies, 211, 214;
carried by leeches, 209;

carried by lice, 125;
carried by mosquitoes,
217; carried by ticks, 232

Dispersal, 135, 164

Distribution :

alpine-boreal, 1 1 1 ; cir-
cumpolar, in; discon-
tinuous, 133, 142, 233;
geographical, 147, 214;
zonal, 85; of fleas, 81-89;
of feather lice, 146; of
nidicoles, 247

Diurnal periodicity, 185

Diversity of form, lice, 1 19

Dove-cotes, 231

Dreys, 91

Dung, see Faeces

Dwarf males, 39, 52, fig.

P- 234
Dysentery, 174

Ectoparasites, 7, 44

Eel-grass, 12, 202

Eggs :

alike, 54; bacteria in, 120,
236, 238; blackflies', 219;
bugs', 247; climate and,
69; cuckoo's, 38, 257,
262-264; destroyed, 18,
28 ; duck's, 237 ; em-
bryonated, 181, 188 ;
feather lices', 123, ferti-
lisation of, 65 ; fertility of,
44; fixing of, 69; gnats',
215; hatching, 70, 123;
laid in hosts' absence, 112;
laying of, 70, 132, 212;
laying reduced, 37, 217;
mites', 225; number of,
38, 70, 180, 188, 191, 216,
230, 232, 258; parasites',
38; parthenogenetic, 40,
123; poisonous, 232;
shape of fleas', 70; skuas',

254

Encephalitis, 225

Endoparasites, 7, 42, 44

Enemies :

host as, 103, 126, 222;
of blackflies, 219; of fleas,
103; of flies, 222; of
mosquitoes, 217

Environment, 7 :

bird is flea's, 84; constant,
100, 140 ; encourages
adaptation, 182; prey and
7; feather louse, 57, 129;
nests ideal, 19; no adapt-

ation to new, 53 ; response
to, 144; social, 49; stable,
of lice, 59

Enzymes, 74, 242

Epidemics, 36, 53, 169, 237,
240

Epipharynx, 74

Ethology, 146

Evolution : 47-55

of birds, 99, 129, 140, 193;
of bird fleas, 89; conver-
gent, 96, 133, 134, 144,
145; of feather lice, 59,
129, 138, 139, 140; of
fleas, 60; of genitalia, 65;
of host and parasite, 164;
interest in, 4; of nema-
todes, 182; parallel, 62,

132, 134. i44>. H5, 207,
224; of parasitic worm
176; of parasitism, 47-55,
of physiological race, 691
sexual reproduction in,
41; trends in, 94, 116,

Examination of lice, 147
Excretory organ, flea's, 64,

flukes' 198, 200
Exhaustion, of parasite, 38
Exoskeleton, 62, 106
Eyelids, flukes below, 2, 207
Eyes, 3 :

feather lice, 122; fleas',
62, 77; inflamed, 240;
larval fluke in, 207; lost,
97; nematode in, 184

Faeces, 13, 48, 50, 71, 161,

172, 176, 177, 189, 191,

i97> 243, 251, 252
Fasting, see Abstinence
Fauna, nidicolous, 19, 245

252
Fear of mosquitoes, 215
Feathers :

eaten, 3, 50, 57, 118, 119;

exudate of, eaten, 222;

pith eaten, 225; structure

of, 137;

Feeding :

feather lice, 120; fleas',
74-76; -spots, 75

Females, 49 :

cuckoo, 256; feather lice,
123; flea, 63, 64; f. sex
parasitic, 49; genitalia,
65; gnat, 215; hatch first,
78; mites attracted by.

GENERAL INDEX

299

104; outliving males, 73,
79; outsize, 182; para-
sitized by males, 40;
polymorphic, 114; pro-
tecting offspring, 212;
sedentary, 58, 75

Fertility, 44

Fever, relapsing, 225, 232

Fidgeting of host, 33

Fights of cuckoos, 260

Filariasis, 217

Fishermen, 16

Fission :

binary, 236; multiple, 161

Fixing of eggs, 69, 123, 212

Flagellum, 170, 235

Flattening of body :

of bugs, 248; of fleas, 57;
of lice, 57, 119; of louse-
flies, 212

Flocks, 21, 25, 202

Flowers, symbiosis and, 28

Food, 3, I'o, II, 58, 72, 173,
183, 198, 248

Form, diversity of, 119

Formic acid, 127

Fossils, 54, 141, 215

Fosterers, 36, 258-262

Gall, 48 :

-bladder, 3
Gapes, 41, 181
Genal comb, 62
Genera, primitive, 143
Genitalia :

of flea, 65 ; of lice, 140
Gentes, 258
Geographical :

distribution, 147, 214;

history, 100; races, 85,

87, 113
Geological record, 48, 141,

215
Geotropism, 78

Gills, II

Gizzard, 184, 185, 256

Glacial periods, 87

Glands :

cystogenous, 204; pene-
tration, 32; stomach, 184;
uropygidial, 209

Granules in crop, 120

Grazing :

symbiosis and, 21, 23;
tapeworms and, 197

Grouse disease, 222

Gynaecophorus canal, 39,
206

Habitats of flukes, 199

Haemorrhage, 31

Halteres, 21 1

Hatching, 70, 123

Hermaphrodites, 40, 53,
191, 209

Hibernation, 97, 114, 217,
252

Hitch-hiking, 18, 98, 222,
228, 248

Host :

abnormal, 93, 95; cas-
tration of, 31; changing,
92, 93, 116; death oi {see
Death); defence by, 79;
distribution of, 84, 146;
eating fleas, 103; effects
on, 30-37, 186-187; find-
ing of, 38, 42, 213; habits
of, 33 ; haemorrhage in,
31; injuries to, 4, 31, 74>
125; phylogeny of, 141,
142, 164, 193; pigmenta-
tion of, 32; -preference,
100, loi, 189, 222; re-
sistance of, 33; sharing
parasites, 59 ; smell of,
76 ; -specificity, 43, 44,
45, 46, 58, 70, 100, 135,
168, 202 ; wounding of, 74

Host-specificity, 43-46 :
in bird fleas, 100; in
feather lice, 135; in mam-
mal fleas, 70; in Proto-
zoa, 168; in Tapeworms,
45, 193; in Flukes, 202

Hunger of parasites, 38

Hunting, symbiotic, 25

Hybrids, 247

Hyperparasites, 103, 128,
197,217,243

Hyphae, 242

Hypopus, 104, 227

Ice ages, 87, 89
Identification of lice, 147
Ignorance, 145, 156, 246
Immunity, 34, 99 :

birds', 163; ducks', iii;

horses', 76; molluscs',

200; partial, 34; swans'

102
Infection, virulent, 37
Infestation, secondary, 143
Influenza, 36, 44
Injuries, 4, 31, 74, 125
Instinct, 212, 252, 266, 267
Integument, fleas', 56

Intermediate hosts {see also
Vectors) :

amphipods as, 204; am-
phibians as, 207; ants as,
197; arthropods as, 172;
beetles as, 197; birds as,
190; cockroaches as, 184;
copepods as, 195; Crus-
tacea as, 184, 188, 194,
204, 207; dragonfly as,
204; earthworm as, 184,
186; fish as, 32, 183, 194,
201, 202, 203, 206-207 ;
fleas as, 98, 103, 177; flies
as, 1 97; freshwater shrimps
as 185, 186, 195; func-
tion of, 1 78 ; grasshoppers
as, 183; hog-slaters as,
190; Hydrobia as, 202;
insects as, 188, 195, 207;
leeches as, 209; lice as,
125; mammals as,; 184
mites as, 197; molluscs as,
2,0, i95> i97> .205, 206,
207; multiplicity of, 42;
mussels as, 30; ostracods
^s, 195; periwinkles as,
204; sand-hoppers as,
204; shore crabs as, 204;
vertebrates as, 232; water
fleas as, 184, 195; weevils
as, 185; woodlice as, 184;
worms as, 195; of worms,

177
Iron necessary, 72
Islands, 45, 46, 52, 90, 138
Isolation, 45, 85, 90, 133,

138

Jargon, 106

Keratin, 120, 250
Kidneys, 3
Kissing, 42

Labium, 74

Lacinia, 74

Larvae, 9, 47 :

acanthella, 189; black-
flies', 219; budding of, 39;
clothes moths', 250; cysti-
cercus, 192, 195; Diplo-
stomulum, 207; emer-
gence of, 71; food of, 58,
72; free, of flea, 57;
houseflies' 221 ; host speci-
fic, 45; infected, 232;
louseflies', 213; mites'.

300

FLEAS, FLUKES AND CUCKOOS

224; moulting of, 71;
mouth-parts of, 71; nests,
in, 61, 247; parasitic, 55;
parasitised, 251; predac-
ious, 50; procercoid, 194;
scavenging, 251; suited
by nests, loi ; suppres-
sion of, 43; Tetracotyle,
206; tongue-worms', 23 ;3
worms', 176

Leap of flea, 77, 78

Legs :

flea, 58, 77; lice, 58, 122;
lost, 41 ; vestigial 233

Lemon juice, 127

Length of tapeworm, 191

Leprosy, 98

Leucocytes, 168, 173

Licking, 42

Life-cycle :

Ascaris, 1 80 ; Capillaria,
186; Cryptocotyle,202>', fig-
5, p. 203; Echinostomes,
205; ectoparasites, 178;
fleas, 68; flukes, 178,
198-208; gnats, 216;
Heterakis, 183; insects, 68;
leeches, 209; lice, 123;
midges, 220; Oxyspirura,
184; parasites, 47 ; Plas-
modium, 1 65 ; Prosthogoni-
mus, 204; Roundworms,
179-186; Sporozoa, 160 ;
Strigeoidea, 206; Strongy-
lina, 182; Syngamus, 181;
tongue-worms, 233; tape-
worms, 194-197

Life-cycles :

contrasting, 9; complex,
42; duration of, 73, 112;
simple, 43

Light, reaction to, 164

Liver, 3, 173

Locomotion, 121

Longevity, 73, i"i2

Luminous :

bacteria, 239; organs, 239

Lungs, 3, 180, 226, 243

Lymph, 3

Malaria,. 164 170, 214, 217

Males :

asymmetrical, 226; at-
tached to females, 39;
dwarf, 39, 53, 230; dying
before females 68; flea,
64, 68; genitalia, 140;
gnat, 216; parasite of

females, 40; surviving, 54

Mange, 226

Mantle, 30

Marrow, 33, 171

Mating, see Copulation

Measles, 235

Mesmerism, 260

Metacercaria, 206

Metabolism aflfected, 31

Metamorphosis, 57, 125, 21 1

Microclimes, 84

Microfilariae, 185

Microhabitats, 245

Microparasites, 36, 235-244

Migrations, 42, 80, 97, 150,
180, 207

Milk, 217

Milk-bottles, 18

Mimicry, 263

Miracidium, 200

Mobbing, 25

Modification, 4; of anten-
nae, 57; of bristles, 96;
of flies, 2 1 1 ; of head, 119;
of lice, 129; of mouth-
parts, 63, 73, 119; views
on, confused, 179

Mole-hills, 13

Mortality :

of cuckoos, 264; of host,
3i-37> 57» 97, 104, 136,
163, 181, 186, 221, 225,
236; of nestlings, 99; of
parasites, 38

Mother of pearl, 30

Moults, 57, 71

Mountain ash, 12

Mouth, 3, II, 41, 119, 160,
198, 209, 232

Mouth-parts :

armature of, 41 ; bugs',
248; feather lice's, 119;
fleas', 62; gnats', 216;
hypopus, 228; leeches',
209; mites', 227; ticks',
229, 230

Movement :

of fleas, 77; of lice, 122,
132; of louse-flies, 212

Mud-flats, 198

Muscles, 3, 243

Mutations, 52

Mycelium, 242

Mycosis, 243

Mysteries, of cuckoo, 259

Nagana, 172

Nasal cavities, 3, 225, 232

Natural selection, 52

Nectar, 7, 49

Nerve cord, flea, 64

Nesting association, 16, 23,
26, 27

Nesting sites, 10, 102

Nests :

beetles in, 50, 245-252;
bugs in, 247-248; carton,
14; cliff'-swallows, 14;
crows, 246; Dermestids in,
248; deserted, 97, 260;
domed, 14; dry, 94;
ducks', 15; emptied, 261,
268; eyes lost in, 97;
fleas collected from, 61,
72; -flies, 220; fly larvae
in, 251; ground, 91, loi;
hibernation in, 252; house
martins, 16; ideal envir-
onment in, 19 ; moths in,
250; mud, 102; numbers
in, 72, 245, 247; ospreys',
14; owls', 246; parasites in,
7; ptarmigans', 15; rocky,
87; sand martins', 80;
scavengers in, 251; spar-
rows', 85; swallows', 16;
sw^ifts', 213; temperature
of, 249; verminous, 246;
voles', 69; weavers', 14;
wet, 87, loi

Niche, ecological, 131, 133,

139
Nostril, fleas in, 49

Numbers :

effects of large, 32; of
eggs, 38, 69; of fleas, 58;
of fleas per bird, 61, 75;
per nest, 61, 72, 245, 247;
per rat, 68; sand-martin,
80; of individuals, 54; of
feather lice, 58 ; of mam-
mal fleas, 89; of parasites
per host, 3; of Protozoa,
159; of roundworms, 178;
of species, 53, 138

Nymphs, 57, 125, 205

Oceanic islands, 45, 46, 52,
90, 138

Ocelli, 77

Oocyst, 161

Operculum, 123

Orders, 106

Organs :

of attachment, 41 ; of
locomotion, lost, 41

GENERAL INDEX

301

Origin of bird fleas, 89 :
feather-lice, 129, 131;
parasitism, 49; pigeon,
no

Overparasitisation, 37

Paludrine, 164

Parasites:

accidental, 9; asexual re-
production of, 39; bud-
ding in, 39; chances of,
38; copulation of, 39;
death of, 38; defined, 6;
dwarf males of, 39; effect
of, on hosts, 30 37; eggs
of, 38; encystmcnt of,
39; evolution of, 47-55,
1 44 ; exchange of, no;
facultative, 9, 10, 221,
251; fleas', 103; herma-
phroditism of, 40; host-
specific, 43; hunger in,
38; intermediate hosts of,
41-43; life a gamble for,
38; life cycles of, 42; loss
of legs of, 41 ; mating of,
39; micro- , 36; modifica-
tions of, 47, 51 ; mouths of,
41 ; numbers of, 3, 38, 54;
obligate, 7, 45; organs of
attachment, 41; parthen-
ogenesis in, 40 ; periodical,
8; permanent, 7; phylo-
geny of, 141; placental,
55; polyembryony in, 40;
predator and, 6; repro-
duction of, 39, 53; re-
striction of, 43, 44, 46, 58;
sense organs of, 42 ; sexual
reproduction in, 39; spec-
ialisation of, 43; strobilis-
ation in, 39 ; temporary, 8,
208; transference of, 42;
tropisms of, 42; variation
in, 36, 51; vectors of, 42

Parasitism : 6-10

adjustments in, 35; ad-
ventitious, 266; brood",
9> 36, 38, 256-268; clep-
to-, 10, 253-255; con-
sequences of, 6, 55; de-
pendence and, 54; devel-
opment of, 4, 48; effects
of, on host,30-37; effects
of, on parasite, 38-46;
evolution of, 47-55; muta-
tions and, 52; natural
selection and, 52; oppor-

tunity for, 49; origin of,
224, 266; pre-adaptation
to, 50>.52; super-, 35

Parapodia, 234

Parthenogenesis, 40, 123,
182, 206, 225

Pastures, symbiosis in, 24

Pearls, 30

Penetration glands, 32

Penicillin, 244

Penis, flea's, 65
of cattle, 175

Petroleum, 48

pH, 192

Phagocytes, 33

Phoresy, 4, 18, 98, 136, 157,
228 {see also hitch-hiking).

Fig. p. 157

Phototropism, 77, 122

Phylogeny, 141

Physogastry, 222

Pigeon lofts, 231

Pigment, 32

Pig-sty, 16

Piracy, 254

Pith, eaten, 225

Placental parasite, 55

Plague, 1,99, 103

Plough and commensals, 1 7

Pneumonia, 240

Polyandry, 267

Polyembryony, 40, 182

Polygamy, 267

Polymorphism, 114, 171

Population, limitation of,
125, 128

Pork, measly, 186

Pox, avian, 241

Pre-adaptation, 52 53 :
of bugs, 248; of birds'
fleas, 103; of elephant's
trunk, 51; of leech's
sucker, 51; of louse flies,
52 ; of mites, 224 ; of Nema-
todes, 179; to nidicolous
life, 103; to parasitism, 52,
of squirrels' fleas, 91

Predators, 6, 50

Preening, 33, 103, 126

Primitive characters, 132

Proboscis, 190, 214

Progenesis, 177

Promiscuity, 264, 267

Pronotal comb, 62, 96

Protein, 183

Proventriculus, 183

Pseudopodium, 174

Psittacosis, 240

Psychological relations, 12,

Pullorum disease, 237

Pupae :

of blackflies, 219 ; of
fleas, 57, 72, 73; in nests,
61

Pygidium, 77

Quarries, 1 1 4

Quotations :

Addison 129, Andersson
in Bannerman 21, 22,
Aristotle 72, Bacon, Fran-
cis 105, Bible see Bible,
Browning, Robert 30, Buf-
fon 176, Cervantes 118,
Chandler, A. C, 164
Chisholm, A. H. 127,
Coleridge, S. T. 253,
Condry 127, Davies, W.
H. 1 7, de Morgan, Augus-
tus (modern version) 103,
Denny, Henry 118, Elton,
C. S. 18, Franklin, Ben-
jamin 125, Gains 38,
Gray, Thomas 16, Herod-
otus 20, Hill 108, Hirst,
L. F. 106, Hooke, Dr.
61, Huxley, J. S. 54.
Johnson, Dr. 56, Jonson,
Ben 6, Lucretius 44, Mitz-
main M.B., 104, Mouffet,
Thomas 210, 211, 213,
214, 218, 224, 226, 229,
Pennant, Thomas 2 1 , Pliny
23, 30, 68, 127, 208, 259,
262, Shakespeare, William
16, 220, 245, Shipley, A.E.
3, 220, Snodgrass, R. E.
60, 65, Somerville, Wil-
liam 2, Spenser, Edmund
47, Waterston, J. 79, 245

Races, geographical, 85, 87,

"3
Raft, gnats' egg-, 215
Range, extension of, 87, 109
Reactions of host, 4, 33, 125,

128
Receptaculum seminis, 66,

109, 113
Record, fossil, 48, 54, 141
Redia, 200

Relapsing fever, 225, 238
Relations, psychological, 12,

302

FLEAS, FLUKES AND CUCKOOS

Releaser, 259

Reproduction :

asexual, 39, 161; fungal,
242; hermaphrodite, 40;
parthenogenetic, 40, 123,
182, 206, 225; sexual, 39

Resistance of host, 32-34

Respiration :

anaerobic, 1 92 ; cutaneous,
232; tracheal, 63

Restriction of parasite :
to head, 58; to one host,
58; to one order, 130

Ringworm, 242

Rostrum of tick, 229

Saliva, 31, 74, 219, 232
Saltings, 199
Sand, 114

Saprophytes, 236,242, 251
Sarcoma, 241
Scabies, 226
Scaly-leg, 226
Scattering of eggs, 70
Scavengers, 51, 121, 251
Scent of host, 76
Schizogony, 161, 163;

exoerythrocytic, 165
Scolex, 191
Seasons and fleas, 68
Sedentary habit, 116
Seed-ticks, 230
Sense-organs :

lice, 121; lost, 42
Senses, fleas', 75
Sentinels, 15, 21
Sexes, proportion of, 79;

dimorphism of, 167, 179
Sexual reproduction, 39
Sites of infection, 3, 8,

Fig. I p. 8
Size: fleas', 62; lice's 119;

parasites' 50
Skin, 3

Sleeping sickness, 98, 1 72
Smallpox, 241
Soup, flea in, 112
Specialisation, 46, 212
Speciation, 45, 85, 133, 137
Species, 107, 108
Specificity :

ethological, 45, 146; host,

43 46; phylogenetic, 44,

Spermathecae, 65

Spermatozoa, 65

Spines, 41, 74, 78, 122,

190-191
Spiracles, 63
Spleen, 33
Spores, 42, 103, 236, 242,

243

Sporocyst, 204, 206

Stables, 16

Starvation, 75

Strength, flea's, 78

Strobila, 192

Strobilisation, 39, 182

Sub-species, 85, 90, 116

Success: of fleas and lice, 59;
of cuckoos, 2

Suckers, 41, 52, 104, 159,
191, 194, 198, 208, 228,
229

Super-families, 106

Superparasitism, 35

Survival, 97

Susceptibility :

of Culex, 217; of old birds,
237; of Passerines, 165

Swarms, flea, 80

Swimmers' itch, 206

Symbiosis, 4, 20-29 :

in ants' nests, 5 1 ; bacteria
and, 121, 239; defined,
20; delousing and, 22; in
flocks, 21 ; flowers and, 28;
fungi and, 242 ; in grazing,
21, 23; in hunting, 25;
mites and, 227; moths
and, 251; nidicoles and,
249; wasps and, 26

Symphiles, 51, 238

Synsacrum, 261

Synthesis by bacteria, 239

Syphilis, 238

Systematics, 106, 147

Temperature, attractive, 76 ;
birds' nests', 80; effects of,
137; fleas' eggs and, 70;
life cycle and, 70, 124

Termitaries, 13, 51

Territory, birds', 257

Throat-pouches, 3, 121

Tolerance, 29

Toxins, 31, 32, 231

Tracheae, fleas', 63

Transference, 116, 135, 160
Transport hosts, 43, 135,

163, 181, 183, 189, 228
Tropisms, 42, 77, 78
Tuberculosis, 31, 236-237
Typhus, 98

Umbilical cord, 13
Uropygidial glands, 209

Vaccination, 241

Vagina, 40, 173

Varieties, 81, 85

Vectors {see also intermedi-
ate hosts) : arthropods as,
172; blackflies as, 219;
fleas as, 98, 172; flies as,
172; insects as, 240;
leeches as, 31, 209; louse
flies as, 1 72 ; mosquitoes as,
165, 217, 241; multiple,
178; red mites as, 172,
238; ticks as, 232; viruses
and, 240

Vermicules, 1 65

Vibrio infection, 239

Vinegar, 48, 127

Virulence of infection, 36

Viruses, 240-241

Vitamins, 183, 193, 239

Viviparity, 212

Walnut, 127
Warmth, attractive, 75
Weather, 34
Wing buds, 73
Wings :

cast off", 41, 213, 222;

lost, 213, 248; molluscs

under, 18; reduced, 52,

213
Wounds :

caused by leeches, 209;

of birds, 187; of hosts, 74,

99; parasitism and, 23;

symbiosis and, 22

Yaws, 238
Yellow fever. 217

Zones of distribution, 85,
loi, 217

SCIENTIFIC NAMES OF BIRDS
MENTIONED IN THE TEXT

Accipiter nisuSj see Sparrow-
Hawk
Acrocephalus schoenobaenus, see

Sedge-Warbler
Acrocephalus scirpaceus, see

Reed-Warbler
Actitis hypoleucos, see Common

Sandpiper
Aegithalos caudatus, see Long-
tailed Tit
Alauda arvensis, see Sky-Lark
Alca tarda, see Razorbill
Alcedo atthis, see Kingfisher
Alle alle, see Little Auk
Anas acuta, see Pintail
Anas americana, see American

Wigeon
Anas crecca, see Teal
Anas penelope, see Wigeon
Anas platyrhyncha, see Mallard
Anas querquedula, see Gar-

ganey
Anas strepera, see Gadwall
Anser brachyrhynchus , see Pink-
footed Goose
Anthus pratensis, see Meadow-
Pipit
Apus apus, see Swift
Aquila chrysaetus, see Golden

Eagle
Archilochus colubris, see Ruby-
throated Humming-bird
Ardea cinerea, see Heron
Ardea purpurea, see Purple

Heron
Ardeola ibis, see Buff-backed

Heron
Arenaria inter pres, see Turn-
stone
Asio flammeus, see Short-
eared Owl
Asio otus, see Long-eared Owl
Athene noctua, see Little Owl
Aythyaferina, see Pochard
Aythya fuligula, see Tufted

Duck
Aythya marila, see Scaup

Bombycilla garrula, see Wax-
wing

Bonasa umbellus, see Ruffed
Grouse

Botaurus stellaris, see Bittern

Branta bemicla, see Brent
Goose

Branta leucopsis, see Barnacle-
Goose

Branta ruficollis, see Red-
breasted Goose

Bucephala clangula, see Golden-
eye

Burhinus oedicnemus, see Stone-
Curlew

Cacicus cela, see Yellow-
backed Oriole
Calidris alpina, see Dunlin
Calidris maritima, see Purple

Sandpiper
Calandrella dukhunensis, see

Lark
Capella gallinago, see Snipe
Caprimulgus europaeus, see

Nightjar
Carduelis cannabina, see Linnet
Carduelis carduelis, see Gold-
finch
Carduelis flammea, see Redpoll
Carduelis spinus, see Siskin
Charadrius hiaticula, see

Ringed Plover
Chenopis atrata, see Australian

Black Swan
Chionis alba, see Sheath-bill
Chlidonias hybrida, see Whis-
kered Tern
Chloris chloris, see Greenfinch
Ciconia ciconia, see White

Stork
Cinclus cinclus, see Dipper
Clamator coromandus, see Red-
winged Crested Cuckoo
Clamator glandarius, see Great

Spotted Cuckoo
Clangula hyemalis, see Long-
tailed Duck
Coccyzus americanus, see Yel-
low-billed Cuckoo
Columba livia, see Rock-Dove
Columba oenas, see Stock-
Dove
Columba palumbus, see Wood-
Pigeon
Colymbus arcticus, see Black-
throated Diver

Colymbus immer, see Great

Northern Diver
Colymbus stellatus, see Red-
throated Diver
Coracias garrulus, see Roller
Corvus brachyrhynchus, see Fish-
Crow
Corvus corax, see Raven
Corvus cornix, see Hooded Crow
Corvus corone, see Carrion-

Crow
Corvus frugilegus , see Rook
Corvus monedula, see Jackdaw
Corvus ossifraga, see Eastern

Crow
Coturnix coturnix, see Quail
Crex crex, see Corn- Crake
Crocethia alba, see Sanderling
Cuculus canorus, see Cuckoe
Cygnus olor, see Mute Swan

Dryobates major, see Great
Spotted Woodpecker

Emberiza citrinella, see Yellow

Hammer
Erithacus rubecula, see Robin
Eupsittula canicularis, see Par-

rakeet

Falco columbarius, see Merlin
Falco mexicanus, see Prairie

Falcon
Falco peregrinus, see Peregrine

Falcon
Falco rusticola, see Greenland

Falcon
Falco subbuteo, see Hobby
Falco tinnunculus, see Kestrel
Fratercula arctica, see Puffin
Fringilla coelebs, see Chaffinch
Fringilla montifringilla, see

Brambling
Fulica atra, see Coot
Fulmarus glacialis, see Fulmar
Furnarius rufus, see Oven-

Bird

Gallinula chloropus, see Moor-
hen
Callus domesticus, see Fowl
Callus gallus, see Jungle-Fow
Garrulus glandarius, see Jay

304

FLEAS, FLUKES AND CUCKOOS

Haematopus ostralegus, see

Oyster-Catcher
Haliaedus albicilla, see White-
tailed Eagle
Haliaedus leucocephalus , see

Bald Eagle
Heteronetta atricapilla, see

South American Duck
Hierococcyx varius, see Indian

Hawk-Cuckoo
Himantopus himantopus, see

Black-winged Stilt
Himatopus mexicanus, see

Black-necked Stilt
Hirundo rustica, see Swallow
Hirundo rustica erythrogaster ,

see Barn-Swallow
Hydrobates pelagicus, see

Storm-Petrel

Jynx torquilla, see Wryneck

Lagopus mutus, see Ptarmigan

Lagopus scoticus, see Grouse

Lampromorpha caprius, see
Small Golden Cuckoo

Lanius collurio, see Red-
backed Shrike

Larus argentatus, see Herring-
Gull

Larus canus, see Common Gull

Larus dominie anus , see
Dominican Gull

Larus hyperboreus, see Glau-
cous Gull

Larus marinus, see Greater
Black-backed Gull

Larus pipixcan, see Franklin's
Gull

Larus ridibundus, see Black-
headed Gull

Leptoptilos crumeniferus , see
Marabou Stork

Leucopolius alexandrinus , see
Kentish Plover

Limosa lapponica, see Godwit

Loxia curvirostra, see Crossbill

Lymnocryptes minimus, see^dick
Snipe

Martula urbica, see House-
Martin

Mergus albellus, see Smew

Mergus merganser, see
Goosander

Mergus serrator, see Mergan-
ser and Red-breasted
Merganser

Merops nubicus, see Carmine
Bee-eater

Alolothrus badius, see Bay-
winged Cow-bird

Alolothrus rufo-axillaris, see
Screaming Cow-bird

Alonticola saxatilis, see Rock-
Thrush

Alotacilla alba, see Pied Wag-
tail and White Wagtail

Alotacilla flava, see Yellow
Wagtail

Aiuscicapa hypoleuca, see Pied
Flycatcher

Nestor notabilis, see Kea
Nucifraga caryocatactes , see

Nutcracker
Numenius arquata, see Curlew
Numenius borealis, see Es-

quimo Curlew
Numida meleagris, see Guinea

Fowl

Oenanthe oenanthe, see Wheat-
ear

Oriolus oriolus, see Golden
Oriole

Pagophila eburnea, see Ivory

Gull
Pandion haliaetus, see Osprey
Panurus biarmicus, see Bearded

Tit
Parus atricapillus, see Willow-
Tit
Parus caeruleus, see Blue Tit
Parus cristatus, see Crested

Tit
Parus major, see Great Tit
Passer domesticus, see Sparrow
Pastor roseus, see Rose-
coloured Pastor
Pavo cristatus, see Peacock
Pelecanoides urinatrix, see

Diving Petrel
Perdix perdix, see Partridge
Pernis apivorus, see Honey-

Buzzard
Petrochelidon albifrons, see Cliff-
Swallow
Phalacrocorax aristotelis, see

Shag
Phalacrocorax carbo, see Cor-
morant
Phalaropus fulicariuSf see Grey
Phalarope

Phalaropus lobatus, see Red-
necked Phalarope

Phasianus colchicus, see
Pheasant

Phoenicurus ochrurus, see Black
Redstart

Phoenicurus phoenicurus, see
Redstart

Phylloscopus collybita, see Chiff-
chaff

Phylloscopus sibilatrix, see
Wood-Warbler

Pica pica, see Magpie

Picus viridis, see Green Wood-
pecker

Platalea leucorodia, see Spoon-
bill

Platycercus unicolor, see Parra-
keet

Pluvanius aegyptius, see Croco-
dile-Bird

Podiceps cristatus, see Great
Crested Grebe

Podiceps nigricollis, see Black-
necked Grebe

Progne subis, see Purple
Martin

Prunella modularis, see Hedge-
Sparrow

Psephotus chrysopterygius, see
Parrakeet

Pterocnemia pennata, see Rhea

Pteroptochus rubecula, see Cheu-
can

Ptychorhamphus aleuticus, see
Auklet

Puffinus gravis, see Great
Shearwater

Puffinus puffinus, see Manx
Shearwater

Pygoscelis taeniata, see Gentoo
Penguin

Pyrrhocorax graculus, see
Alpine Chough

Pyrrhocorax pyrrhocorax, see
Chough

Pyrrhula pyrrhula, see Bull-
finch

Quiscalus quiscula, see Purple
Grackle

Recurvirostra avosetta, see

Avocet
Regulus regulus, see Goldcrest
Rhea americana, see Rhea
Riparia riparia, see Sand

Martin

INDEX OF SCIENTIFIC NAMES OF BIRDS

305

Rissa tridactyla, see Kittiwake

Saxicola rubetra, see Whinchat
Scolopax rusticola, see Wood-
cock
Sitta europfiea, see Nuthatch
Somateria mollissima, see Com-
mon Eider and Eider-
Duck
Spatula clypeata, see Shoveler
Stercorarius longicaudatus, see

Long-tailed Skua
Stercorarius parasiticus, see

Arctic Skua
Stercorarius pomarinus, see

Pomatorhine Skua
Stercorarius skua, see Great

Skua
Sterna albifrons, see Little Tern
Sterna hirundo, see Common

Tern
Sterna macrura, see Arctic
Tern

Sterna sandvicensis , see Sand-
wich Tern
Streptopelia turtur, see Turtle-

Dove
Strix aluco, see Tawny Owl
Struthio camelus, see Ostrich
Sturnus vulgaris, see Starling
Sula bassana, see Gannet
Sylvia communis, see White-
throat

Tadorna tadorna, see Shcld-
Duck

Teteropis pelzelni, see Slender-
billed Weaver

Tetrao urogallus, see Caper-
caillie

Tringa jlavipes, see Yellow-
shank

Tringa melanoleuca, see
Greater Yellowshank

Tringa ochropus, see Green
Sandpiper

Tringa stagnalilis, see Marsh

Sandpiper
Tringa totanus, see Redshank
Troglodytes troglodytes, see

Wren
Turdus ericetorum, see Song-
Thrush
Turdus merula, see Blackbird
Turdus musicus, see Redwing
Turdus pilaris, see Fieldfare
Tyto alba, see Barn-Owl

Upupa epops, see Hoopoe
Uria aalge, see Guillemot

Vanellus vanellus, see Lapwing

Zenaidura carolinensis , see
Mourning Dove

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